Repetitive blast exposure in mice and combat veterans causes persistent cerebellar dysfunction

Meabon, James S.; Huber, Bertrand R.; Cross, Donna J.; Richards, Todd L.; Minoshima, Satoshi; Pagulayan, Kathleen F.; Li, Ge; Meeker, Kole D.; Kraemer, Brian C.; Petrie, Eric C.; Raskind, Murray A.; Peskind, Elaine R.; Cook, David G.

doi:10.1126/scitranslmed.aaa9585

Cited by 139Traumatic Brain Injury ResearchTraumatic Brain Injury and Neurovascular DisturbancesAutomotive and Human Injury Biomechanics

Repetitive blast exposure in mice and combat veterans causes persistent cerebellar dysfunction

Meabon, James S., Huber, Bertrand R., Cross, Donna J., Richards, Todd L., Minoshima, Satoshi, Pagulayan, Kathleen F., Li, Ge, Meeker, Kole D. +5 more·2016·Science Translational Medicine

DOI 10.1126/scitranslmed.aaa9585

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Abstract

Blast exposure can cause mild traumatic brain injury (TBI) in mice and other mammals. However, there are important gaps in our understanding of the neuropathology underlying repetitive blast exposure in animal models compared to the neuroimaging abnormalities observed in blast-exposed veterans. Moreover, how an increase in the number of blast exposures affects neuroimaging endpoints in blast-exposed humans is not well understood. We asked whether there is a dose-response relationship between the number of blast-related mild TBIs and uptake of (18)F-fluorodeoxyglucose (FDG), a commonly used indicator of neuronal activity, in the brains of blast-exposed veterans with mild TBI. We found that the number of blast exposures correlated with FDG uptake in the cerebellum of veterans. In mice, blast exposure produced microlesions in the blood-brain barrier (BBB) predominantly in the ventral cerebellum. Purkinje cells associated with these BBB microlesions displayed plasma membrane disruptions and aberrant expression of phosphorylated tau protein. Purkinje cell loss was most pronounced in the ventral cerebellar lobules, suggesting that early-stage breakdown of BBB integrity may be an important factor driving long-term brain changes. Blast exposure caused reactive gliosis in mouse cerebellum, particularly in the deep cerebellar nuclei. Diffusion tensor imaging tractography of the cerebellum of blast-exposed veterans revealed that mean diffusivity correlated negatively with the number of…

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Blood-Brain Barrier: From Physiology to Disease and Back
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A network-based neurobiological model of PTSD: evidence from structural and functional neuroimaging studies
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Pathophysiology of Traumatic Brain Injury
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The synapse in traumatic brain injury
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BBB pathophysiology–independent delivery of siRNA in traumatic brain injury
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Induction of a transmissible tau pathology by traumatic brain injury
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Resistance, vulnerability and resilience: A review of the cognitive cerebellum in aging and neurodegenerative diseases
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Low-level blast exposure disrupts gliovascular and neurovascular connections and induces a chronic vascular pathology in rat brain
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Blast exposure elicits blood-brain barrier disruption and repair mediated by tight junction integrity and nitric oxide dependent processes
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Brain and blood biomarkers of tauopathy and neuronal injury in humans and rats with neurobehavioral syndromes following blast exposure
Dickstein, D., Gasperi, R. D., Sosa, M. G., Pérez-García, G., Short, J., Sosa, H., Perez, G. M., Tschiffely, A. E., Dams-O'Connor, K., Pullman, M., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0674-z · Cited by 86 · see citing works
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Chronic traumatic encephalopathy neuropathology might not be inexorably progressive or unique to repetitive neurotrauma
Iverson, G. L., Gardner, A. J., Shultz, S. R., Solomon, G. S., McCrory, P. R., ZAFONTE, R. D., Perry, G. L., Hazrati, L., Keene, C. D., & Castellani, R. J. (2019) · Brain · doi:10.1093/brain/awz286 · Cited by 99 · see citing works
VTA-projecting cerebellar neurons mediate stress-dependent depression-like behaviors
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Blast exposure causes dynamic microglial/macrophage responses and microdomains of brain microvessel dysfunction
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Identifying degenerative effects of repetitive head trauma with neuroimaging: a clinically-oriented review
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ApoE4-associated phospholipid dysregulation contributes to development of Tau hyper-phosphorylation after traumatic brain injury
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Post-Concussion Syndrome and Chronic Traumatic Encephalopathy: Narrative Review on the Neuropathology, Neuroimaging and Fluid Biomarkers
Mavroudis, I. A., Kazis, D. A., Chowdhury, R., Petridis, F., Costa, V., Balmuș, I.-M., Ciobica, A. S., Luca, A.-C., Radu, I., Dobrin, R., et al. (2022) · Diagnostics · doi:10.3390/diagnostics12030740 · Cited by 62 · see citing works
Systems Biology, Neuroimaging, Neuropsychology, Neuroconnectivity and Traumatic Brain Injury
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Neuroradiological Changes Following Single or Repetitive Mild TBI
Kulkarni, P., Morrison, T., Cai, X.-Z., Iriah, S., Simon, N. G., Sabrick, J., Neuroth, L., & Ferris, C. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00034 · Cited by 56 · see citing works
A critical review of radiotracers in the positron emission tomography imaging of traumatic brain injury: FDG, tau, and amyloid imaging in mild traumatic brain injury and chronic traumatic encephalopathy
Ayubcha, C., Revheim, M.-E. R., Newberg, A. B., Moghbel, M. C., Rojulpote, C., Werner, T. J., & Alavi, A. A. (2020) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-020-04926-4 · Cited by 54 · see citing works
Blast-Exposed Veterans With Mild Traumatic Brain Injury Show Greater Frontal Cortical Thinning and Poorer Executive Functioning
Clark, A. L., Merritt, V. C., Bigler, E. D., Bangen, K. J., Werhane, M. L., Sorg, S. F., Bondi, M. W., Schiehser, D. M., & Delano‐Wood, L. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00873 · Cited by 52 · see citing works
How to Translate Time: The Temporal Aspects of Rodent and Human Pathobiological Processes in Traumatic Brain Injury
Agoston, D. V., Vink, R., Helmy, A. E., Risling, M., Nelson, D., & Prins, M. L. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6261 · Cited by 52 · see citing works
A Mouse Model of Repetitive Blast Traumatic Brain Injury Reveals Post-Trauma Seizures and Increased Neuronal Excitability
Bugay, V., Bozdemir, E., Vigil, F. A., Chun, S. H., Holstein, D. M., Elliott, W. R., III, Sprague, C., Cavazos, J. E., Zamora, D. O., Rule, G. T., et al. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6333 · Cited by 52 · see citing works
Nitric oxide synthase mediates cerebellar dysfunction in mice exposed to repetitive blast-induced mild traumatic brain injury
Logsdon, A. F., Schindler, A. G., Meabon, J. S., Yagi, M., Herbert, M. J., Banks, W. A., Raskind, M. A., Marshall, D. A., Keene, C. D., Perl, D. P., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-66113-7 · Cited by 49 · see citing works
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Alterations in Plasma microRNA and Protein Levels in War Veterans with Chronic Mild Traumatic Brain Injury
Ghai, V., Fallen, S., Baxter, D. H., Scherler, K., Kim, T., Zhou, Y. F., Meabon, J. S., Logsdon, A. F., Banks, W. A., Schindler, A. G., et al. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2019.6826 · Cited by 45 · see citing works
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Time Window of Head Impact Kinematics Measurement for Calculation of Brain Strain and Strain Rate in American Football
Liu, Y., Domel, A. G., Cecchi, N. J., Rice, E. N., Callan, A. A., Raymond, S., Zhou, Z., Zhan, X., Li, Y., Zeineh, M., et al. (2021) · Annals of Biomedical Engineering · doi:10.1007/s10439-021-02821-z · Cited by 43 · see citing works
Behavioral and inflammatory response in animals exposed to a low-pressure blast wave and supplemented with β-alanine
Hoffman, J. R., Zuckerman, A., Ram, O., Sadot, O., Stout, J. R., Ostfeld, I., & Cohen, H. (2017) · Amino Acids · doi:10.1007/s00726-017-2383-8 · Cited by 41 · see citing works
Disrupted Gamma Synchrony after Mild Traumatic Brain Injury and Its Correlation with White Matter Abnormality
Wang, C., Costanzo, M. E., Rapp, P. E., Darmon, D. M., Nathan, D. E., Bashirelahi, K., Pham, D. L., Roy, M. J., & Keyser, D. O. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00571 · Cited by 38 · see citing works
Modeling the Long-Term Consequences of Repeated Blast-Induced Mild Traumatic Brain Injuries
Agoston, D. V. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2017.5317 · Cited by 38 · see citing works
Repeated mild blast exposure in young adult rats results in dynamic and persistent microstructural changes in the brain
Badea, A., Kamnaksh, A., Anderson, R. J., Calabrese, E., Long, J. B., & Agoston, D. V. (2018) · NeuroImage Clinical · doi:10.1016/j.nicl.2018.01.007 · Cited by 37 · see citing works
Modulation of Post-Traumatic Immune Response Using the IL-1 Receptor Antagonist Anakinra for Improved Visual Outcomes
Evans, L. P., Woll, A. W., Wu, S., Todd, B. P., Hehr, N., Hedberg‐Buenz, A., Anderson, M. G., Newell, E. A., Ferguson, P. J., Mahajan, V. B., et al. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2019.6725 · Cited by 37 · see citing works
Animal model of repeated low-level blast traumatic brain injury displays acute and chronic neurobehavioral and neuropathological changes
Ravula, A. R., Rodriguez, J., Younger, D., Perumal, V., Shao, N., Rao, K. V. R., Pfister, B. J., & Chandra, N. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113938 · Cited by 38 · see citing works
Retrospective and Prospective Memory Among OEF/OIF/OND Veterans With a Self-Reported History of Blast-Related mTBI
Pagulayan, K. F., Rau, H., Madathil, R. L., Werhane, M. L., Millard, S. P., Petrie, E. C., Parmenter, B. A., Peterson, S., Sorg, S. F., Hendrickson, R. C., et al. (2017) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617717001217 · Cited by 35 · see citing works
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Progressive Cognitive and Post-Traumatic Stress Disorder-Related Behavioral Traits in Rats Exposed to Repetitive Low-Level Blast
Garcia, G. S. P., Perez, G. M., Gasperi, R. D., Sosa, M. G., Otero-Pagan, A., Pryor, D., Abutarboush, R., Kawoos, U., Hof, P., Cook, D., et al. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2020.7398 · Cited by 30 · see citing works
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Structural disruption of the blood–brain barrier in repetitive primary blast injury
Uzunallı, G., Herr, S., Dieterly, A. M., Shi, R., & Lyle, L. T. (2021) · Fluids and Barriers of the CNS · doi:10.1186/s12987-020-00231-2 · Cited by 37 · see citing works
A Comprehensive Review of Experimental Rodent Models of Repeated Blast TBI
Skotak, M., Townsend, M. T., Ramarao, K. V., & Chandra, N. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.01015 · Cited by 34 · see citing works
Concussion induces focal and widespread neuromorphological changes.
Sussman, D., da Costa, L., Chakravarty, M., Pang, E., Taylor, M. J., & Dunkley, B. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.04.026 · Cited by 32 · see citing works
Rapid Repeat Exposure to Subthreshold Trauma Causes Synergistic Axonal Damage and Functional Deficits in the Visual Pathway in a Mouse Model
Vest, V. D., Bernardo‐Colón, A., Watkins, D., Kim, B., & Rex, T. S. (2018) · Journal of Neurotrauma · doi:10.1089/neu.2018.6046 · Cited by 32 · see citing works
Behavioral and Myelin-Related Abnormalities after Blast-Induced Mild Traumatic Brain Injury in Mice
Nonaka, M., Taylor, W. W., Bukalo, O., Tucker, L. B., Fu, A. H., Kim, Y., McCabe, J. T., & Holmes, A. (2021) · Journal of Neurotrauma · doi:10.1089/neu.2020.7254 · Cited by 32 · see citing works
Timing matters: Sex differences in inflammatory and behavioral outcomes following repetitive blast mild traumatic brain injury
Baskin, B. M., Logsdon, A. F., Lee, S. J., Foresi, B. D., Peskind, E. R., Banks, W. A., Cook, D. G., & Schindler, A. G. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.03.003 · Cited by 30 · see citing works
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Overpressure Exposure From .50-Caliber Rifle Training Is Associated With Increased Amyloid Beta Peptides in Serum
Thangavelu, B., LaValle, C. R., Egnoto, M. J., Nemes, J., Boutté, A. M., & Kamimori, G. H. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00620 · Cited by 30 · see citing works
Defective methionine metabolism in the brain after repeated blast exposures might contribute to increased oxidative stress
Arun, P., Rittase, W. B., Wilder, D. M., Wang, Y., Gist, I. D., & Long, J. B. (2017) · Neurochemistry International · doi:10.1016/j.neuint.2017.07.014 · Cited by 29 · see citing works
Blast Preconditioning Protects Retinal Ganglion Cells and Reveals Targets for Prevention of Neurodegeneration Following Blast-Mediated Traumatic Brian Injury
Harper, M. M., Woll, A. W., Evans, L. P., Delcau, M. A., Akurathi, A., Hedberg‐Buenz, A., Soukup, D. A., Boehme, N., Hefti, M. M., Dutca, L. M., et al. (2019) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.19-27565 · Cited by 29 · see citing works
Early to Long-Term Alterations of CNS Barriers After Traumatic Brain Injury: Considerations for Drug Development
Rodriguez‐Grande, B., Ichkova, A., Lemarchant, S., & Badaut, J. (2017) · The AAPS Journal · doi:10.1208/s12248-017-0123-3 · Cited by 29 · see citing works
Blast–related disinhibition and risk seeking in mice and combat Veterans: Potential role for dysfunctional phasic dopamine release
Schindler, A. G., Meabon, J. S., Pagulayan, K. F., Hendrickson, R. C., Meeker, K. D., Cline, M. M., Li, G., Sikkema, C. L., Wilkinson, C. W., Perl, D. P., et al. (2017) · Neurobiology of Disease · doi:10.1016/j.nbd.2017.06.004 · Cited by 28 · see citing works
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A mouse Model of Focal Vascular Injury Induces Astrocyte Reactivity, Tau Oligomers, and Aberrant Behavior
Logsdon, A., Lucke-Wold, B., Turner, R., Li, X., Adkins, C., Mohammad, A., Huber, J. D., Rosen, C., & Lockman, P. (2017) · Archives of Neuroscience · doi:10.5812/archneurosci.44254 · Cited by 25 · see citing works
Paclitaxel Reduces Brain Injury from Repeated Head Trauma in Mice
Cross, D., Meabon, J., Cline, M., Richards, T., Stump, A. J., Cross, C. G., Minoshima, S., Banks, W., & Cook, D. (2019) · Journal of Alzheimer's Disease · doi:10.3233/jad-180871 · Cited by 19 · see citing works
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Low-intensity open-field blast exposure effects on neurovascular unit ultrastructure in mice
Li, C., Chen, S., Siedhoff, H. R., Grant, D. G., Liu, P., Balderrama, A., Jackson, M. A., Zuckerman, A., Greenlief, C. M., Kobeissy, F. H., et al. (2023) · Acta Neuropathologica Communications · doi:10.1186/s40478-023-01636-4 · Cited by 26 · see citing works
Neuronal BAG3 attenuates tau hyperphosphorylation, synaptic dysfunction, and cognitive deficits induced by traumatic brain injury via the regulation of autophagy-lysosome pathway
Sweeney, N., Kim, T. Y., Morrison, C. T., Li, L., Acosta, D. M., Liang, J., Datla, N. V., Fitzgerald, J. A., Huang, H., Liu, X., et al. (2024) · Acta Neuropathologica · doi:10.1007/s00401-024-02810-1 · Cited by 27 · see citing works
Repetitive blast mild traumatic brain injury increases ethanol sensitivity in male mice and risky drinking behavior in male combat veterans
Schindler, A. G., Baskin, B. M., Juarez, B., Lee, S. J., Hendrickson, R. C., Pagulayan, K. F., Zweifel, L. S., Raskind, M. A., Phillips, P. E. M., Peskind, E. R., et al. (2021) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14605 · Cited by 26 · see citing works
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Traumatic Brain Injury Biomarkers, Simulations and Kinetics
Hicks, C., Dhiman, A., Barrymore, C., & Goswami, T. (2022) · Bioengineering · doi:10.3390/bioengineering9110612 · Cited by 25 · see citing works
Multi-Modal Signatures of Tau Pathology, Neuronal Fiber Integrity, and Functional Connectivity in Traumatic Brain Injury
Wooten, D. W., Ortiz-Terán, L., Zubcevik, N., Zhang, X., Huang, C., Sepulcre, J., Atassi, N., Johnson, K. A., Zafonte, R., & Fakhri, G. E. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6178 · Cited by 30 · see citing works
Perspectives on repeated low-level blast and the measurement of neurotrauma in humans as an occupational exposure risk
Carr, W. S., Dell, K. C., Yanagi, M. A., Hassan, D. M., & LoPresti, M. L. (2017) · Shock Waves · doi:10.1007/s00193-017-0766-0 · Cited by 23 · see citing works
The Neurovascular Unit as a Locus of Injury in Low-Level Blast-Induced Neurotrauma
Elder, G. A., Sosa, M. A. G., Gasperi, R. D., Garcia, G. S. P., Perez, G. M., Abutarboush, R., Kawoos, U., Zhu, C. W., Janssen, W. G. M., Stone, J. R., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25021150 · Cited by 24 · see citing works
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Authors: Meabon, J. S., Huber, B. R., Cross, D. J., Richards, T. L., Minoshima, S., Pagulayan, K. F., Li, G., Meeker, K. D., Kraemer, B. C., Petrie, E. C., Raskind, M. A., Peskind, E. R., & Cook, D. G.
Affiliations: University of Washington (US)
Boston University (US)
University of Utah (US)
VA Puget Sound Health Care System (US)
Corresponding author: Cook, David G.
ORCID: Meabon, James S.
Huber, Bertrand R.
Cross, Donna J.
Richards, Todd L.
Minoshima, Satoshi
Pagulayan, Kathleen F.
Li, Ge
Meeker, Kole D.
Kraemer, Brian C.
Petrie, Eric C.
Raskind, Murray A.
Peskind, Elaine R.
Cook, David G.
Venue: Science Translational Medicine
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2016-01-13
Volume: 8
Issue: 321
Pages: 321ra6-321ra6
ISSN: 1946-6234 (ISSN-L)
1946-6242
DOI: 10.1126/scitranslmed.aaa9585
OpenAlex: W2235097232
Cited by: 138
References: 100
Citations by year: 2026: 11 · 2025: 3 · 2024: 11 · 2023: 9 · 2022: 11 · 2021: 19 · 2020: 21 · 2019: 15 · 2018: 17 · 2017: 18 · 2016: 3
FWCI: 16.54
Type: journal article
Language: en
Open access: closed
Licence: www.sciencemag.org/about/science-licenses-journal-article-reuse (vor, 366 d)
Locations: Science Translational Medicine (publishedVersion)
PubMed (publishedVersion)
Funders: Department of Veterans Affairs Office of Research
Development Medical Research Service
VA Rehabilitation Research & Development Service
University of Washington Friends of Alzheimer's Research
University of Washington Royalty Research Fund
Northwest Network Mental Illness Research, Education and Clinical Center
Office of Academic Affiliations Advanced Fellowship Program Mental Illness Research and Treatment
Department of Veterans Affairs
NIH (T32 AG000258)
VA Clinical Science R&D Career Development Award Program (#CX00516)
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, cerebellum, combat veterans, Purkinje cells, tau phosphorylation, reactive gliosis, deep cerebellar nuclei, FDG uptake, mean diffusivity, diffusion tensor tractography, dose-response relationship, neuroimaging
MeSH terms: Disks Large Homolog 4 Protein, Animals, Axons, Blast Injuries, Brain Concussion, Cerebellar Diseases, Cerebellum, Gliosis, Glucose, Humans, Male, Membrane Proteins, Mice, Inbred C57BL, Motor Activity, Neuroglia, Neurons, Purkinje Cells, Synapses, Veterans, Fluorodeoxyglucose F18, Guanylate Kinases

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Repetitive blast exposure in mice and combat veterans causes persistent cerebellar dysfunction

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