A critical review of chronic traumatic encephalopathy

Iverson, Grant L.; Gardner, Andrew J.; McCrory, Paul; Zafonte, Ross; Castellani, Rudy J.

doi:10.1016/j.neubiorev.2015.05.008

Cited by 103Traumatic Brain Injury ResearchAlzheimer's disease research and treatmentsTraumatic Brain Injury and Neurovascular Disturbances

A critical review of chronic traumatic encephalopathy

Iverson, Grant L., Gardner, Andrew J., McCrory, Paul, Zafonte, Ross, Castellani, Rudy J.·2015·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2015.05.008

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Abstract

Chronic traumatic encephalopathy (CTE) has been described in the literature as a neurodegenerative disease with: (i) localized neuronal and glial accumulations of phosphorylated tau (p-tau) involving perivascular areas of the cerebral cortex, sulcal depths, and with a preference for neurons within superficial cortical laminae; (ii) multifocal axonal varicosities and axonal loss involving deep cortex and subcortical white matter; (iii) relative absence of beta-amyloid deposits; (iv) TDP-43 immunoreactive inclusions and neurites; and (v) broad and diverse clinical features. Some of the pathological findings reported in the literature may be encountered with age and other neurodegenerative diseases. However, the focality of the p-tau cortical findings in particular, and the regional distribution, are believed to be unique to CTE. The described clinical features in recent cases are very similar to how depression manifests in middle-aged men and with frontotemporal dementia as the disease progresses. It has not been established that the described tau pathology, especially in small amounts, can cause complex changes in behavior such as depression, substance abuse, suicidality, personality changes, or cognitive impairment. Future studies will help determine the extent to which the neuropathology is causally related to the diverse clinical features.

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Most of the gross and microscopic features described as characteristic of CTE have not been independently verified as specific to CTE, and virtually all are associated with aging, other neurological diseases, or both.
“Most of the above-mentioned gross and microscopic features have not, as yet, been independently verified as specific to CTE [27–30], and virtually all are associated with aging, other neurological diseases, or both.”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [29]

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Head Impact Exposure in Youth Football
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Unique Hard Scleral Lens Post‐LASIK Ectasia Fitting
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Neurofibrillary tangles in dementia pugilistica are ubiquitinated.
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Does the Relationship Between Depression and Intimate Partner Aggression Vary by Gender, Victim–Perpetrator Role, and Aggression Severity?
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Mild Cognitive Impairment and Asymptomatic Alzheimer Disease Subjects: Equivalent β-Amyloid and Tau Loads With Divergent Cognitive Outcomes
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Head Impact Exposure in Youth Football: Middle School Ages 12–14 Years
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Retrieval mechanisms for autobiographical memories: Insights from the frontal variant of frontotemporal dementia
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Stressful life events and suicidal behavior in adults with alcohol use disorders: Role of event severity, timing, and type
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Pathologic gambling and bankruptcy
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Increased mortality rate and suicide in S wedish former elite male athletes in power sports
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Intelligence and executive functions in frontotemporal dementia
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Immunocytochemical characterization of glial fibrillary tangles in Alzheimer's disease brain.
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Frequency, magnitude, and distribution of head impacts in Pop Warner football: The cumulative burden
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Interethnic Differences in Dementia Epidemiology: Global and Asia-Pacific Perspectives
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Beta amyloid, tau, neuroimaging, and cognition: sequence modeling of biomarkers for Alzheimer’s Disease
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Sleep-Related Headaches
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Animal models of sports‐related head injury: bridging the gap between pre‐clinical research and clinical reality
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Comparison of clinical characteristics between familial and non-familial early onset Alzheimer’s disease
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Modern Chronic Traumatic Encephalopathy in Retired Athletes: What is the Evidence?
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Considerations for animal models of blast-related traumatic brain injury and chronic traumatic encephalopathy
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Interaction between anxiety, depression, quality of life and clinical parameters in chronic tension‐type headache
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Isoform transition from four-repeat to three-repeat tau underlies dendrosomatic and regional progression of neurofibrillary pathology
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Preclinical Alzheimer disease: identification of cases at risk among cognitively intact older individuals
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Inhibition of Monoacylglycerol Lipase Prevents Chronic Traumatic Encephalopathy-Like Neuropathology in a Mouse Model of Repetitive Mild Closed Head Injury
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4 of the 228 references couldn’t be matched to a known paper.

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White matter and cognition: making the connection
Filley, C. M., & Fields, R. D. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00221.2016 · Cited by 445 · see citing works
Priming the Inflammatory Pump of the CNS after Traumatic Brain Injury
Witcher, K. G., Eiferman, D. S., & Godbout, J. P. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.08.002 · Cited by 222 · see citing works
Long-Term Cognitive and Neuropsychiatric Consequences of Repetitive Concussion and Head-Impact Exposure
McAllister, T. W., & McCrea, M. (2017) · Journal of Athletic Training · doi:10.4085/1062-6050-52.1.14 · Cited by 219 · see citing works
The bidirectional gut-brain-microbiota axis as a potential nexus between traumatic brain injury, inflammation, and disease
Sundman, M., Chen, N., Subbian, V., & Chou, Y. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.05.009 · Cited by 200 · see citing works
Preliminary Study of Plasma Exosomal Tau as a Potential Biomarker for Chronic Traumatic Encephalopathy
Stern, R. A., Tripodis, Y., Baugh, C. M., Fritts, N. G., Martin, B. M., Chaisson, C., Cantu, R. C., Joyce, J. A., Shah, S., Ikezu, T., et al. (2016) · Journal of Alzheimer’s Disease · doi:10.3233/jad-151028 · Cited by 155 · see citing works
Research Gaps and Controversies in Chronic Traumatic Encephalopathy: A Review
Asken, B. M., Sullan, M. J., DeKosky, S. T., Jaffee, M. S., & Bauer, R. M. (2017) · JAMA Neurology · doi:10.1001/jamaneurol.2017.2396 · Cited by 135 · see citing works
Suicide mortality among retired National Football League players who played 5 or more seasons
Lehman, E. J., Hein, M. J., & Gersic, C. M. (2016) · The American Journal of Sports Medicine · doi:10.1177/0363546516645093 · Cited by 112 · see citing works
Helmet efficacy against concussion and traumatic brain injury: a review
Sone, J. Y., Kondziolka, D. S., Huang, J. H., & Samadani, U. (2016) · Journal of neurosurgery · doi:10.3171/2016.2.jns151972 · Cited by 98 · see citing works
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
The behavioral, psychological, and social impacts of team sports: A systematic review and meta-analysis
Zuckerman, S. L., Tang, A. R., Richard, K. E., Grisham, C. J., Kuhn, A. W., Bonfield, C. M., & Yengo-Kahn, A. M. (2021) · The Physician and Sportsmedicine · doi:10.1080/00913847.2020.1850152 · Cited by 98 · see citing works
Factors Influencing Clinical Correlates of Chronic Traumatic Encephalopathy (CTE): a Review
Asken, B. M., Sullan, M. J., Snyder, A., Houck, Z. M., Bryant, V. E., Hizel, L. P., McLaren, M. E., Dede, D. E., Jaffee, M. S., DeKosky, S. T., et al. (2016) · Neuropsychology Review · doi:10.1007/s11065-016-9327-z · Cited by 84 · see citing works
The association between white-matter tract abnormalities, and neuropsychiatric and cognitive symptoms in retired professional football players with multiple concussions
Multani, N., Goswami, R., Khodadadi, M., Ebraheem, A., Davis, K. D., Tator, C. H., Wennberg, R. A., Mikulis, D. J., Ezerins, L., & Tartaglia, M. C. (2016) · Journal of Neurology · doi:10.1007/s00415-016-8141-0 · Cited by 81 · see citing works
Participation in Pre–High School Football and Neurological, Neuroradiological, and Neuropsychological Findings in Later Life
Solomon, G. S., Kuhn, A. W., Zuckerman, S. L., Casson, I. R., Viano, D. C., Lovell, M. R., & Sills, A. K. (2016) · The American Journal of Sports Medicine · doi:10.1177/0363546515626164 · Cited by 79 · see citing works
Concussion—Mild Traumatic Brain Injury
Kamins, J., & Giza, C. C. (2016) · Neurosurgery Clinics of North America · doi:10.1016/j.nec.2016.05.005 · Cited by 79 · see citing works
Football Players' Head-Impact Exposure After Limiting of Full-Contact Practices
Broglio, S. P., Williams, R. M., O’Connor, K. L., & Goldstick, J. E. (2016) · Journal of Athletic Training · doi:10.4085/1062-6050-51.7.04 · Cited by 79 · see citing works
The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features
Iverson, G. L., Keene, C. D., Perry, G., & Castellani, R. J. (2017) · Journal of Alzheimer's Disease · doi:10.3233/jad-170654 · Cited by 72 · see citing works
Chronic Traumatic Encephalopathy: A Brief Overview
Fesharaki‐Zadeh, A. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00713 · Cited by 70 · see citing works
Mild Head Injury☆
Aucone, E. J., Barth, J. T., Freeman, J. R., & Broshek, D. K. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.03098-4 · Cited by 67 · see citing works
Suicide and chronic traumatic encephalopathy
Iverson, G. L. (2016) · The Journal of Neuropsychiatry and Clinical Neurosciences · doi:10.1176/appi.neuropsych.15070172 · Cited by 66 · see citing works
Mild Chronic Traumatic Encephalopathy Neuropathology in People With No Known Participation in Contact Sports or History of Repetitive Neurotrauma
Iverson, G. L., Luoto, T. M., Karhunen, P. J., & Castellani, R. J. (2019) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlz045 · Cited by 63 · see citing works
Accelerated cognitive aging following severe traumatic brain injury: A review
Wood, R. L. (2017) · Brain Injury · doi:10.1080/02699052.2017.1332387 · Cited by 59 · see citing works
Mouse closed head traumatic brain injury replicates the histological tau pathology pattern of human disease: Characterization of a novel model and systematic review of the literature
Kahriman, A., Bouley, J., Smith, T. W., Bosco, D. A., Woerman, A. L., & Henninger, N. (2021) · Acta Neuropathologica Communications · doi:10.1186/s40478-021-01220-8 · Cited by 53 · see citing works
Sports-related concussions: diagnosis, complications, and current management strategies
Hobbs, J. G., Young, J. S., & Bailes, J. E. (2016) · Neurosurgical FOCUS · doi:10.3171/2016.1.focus15617 · Cited by 53 · see citing works
Neurodegenerative Dementias After Traumatic Brain Injury
LoBue, C., Cullum, C. M., Didehbani, N., Yeatman, K., Jones, B., Kraut, M. A., & Hart, J. (2018) · The Journal of Neuropsychiatry and Clinical Neurosciences · doi:10.1176/appi.neuropsych.17070145 · Cited by 51 · see citing works
Chronic traumatic encephalopathy in sports: a historical and narrative review
Solomon, G. S. (2018) · Developmental Neuropsychology · doi:10.1080/87565641.2018.1447575 · Cited by 50 · see citing works
If You're Not Measuring, You're Guessing: The Advent of Objective Concussion Assessments
Broglio, S. P., Guskiewicz, K. M., & Norwig, J. A. (2017) · Journal of Athletic Training · doi:10.4085/1062-6050-51.9.05 · Cited by 45 · see citing works
The Biological Basis of Chronic Traumatic Encephalopathy following Blast Injury: A Literature Review
Aldag, M., Armstrong, R. C., Bandak, F. A., Bellgowan, P. S. F., Bentley, T. B., Biggerstaff, S., Caravelli, K., Cmarik, J. L., Crowder, A. T., DeGraba, T. J., et al. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2017.5218 · Cited by 37 · 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
What Definition Is Used to Describe Second Impact Syndrome in Sports? A Systematic and Critical Review
Stovitz, S. D., Weseman, J. D., Hooks, M. C., Schmidt, R. J., Koffel, J. B., & Patricios, J. (2017) · Current Sports Medicine Reports · doi:10.1249/jsr.0000000000000326 · Cited by 37 · see citing works
Mild Closed-Head Injury in Conscious Rats Causes Transient Neurobehavioral and Glial Disturbances: A Novel Experimental Model of Concussion
Pham, L., Shultz, S. R., Kim, H. A., Brady, R. D., Wortman, R. C., Genders, S. G., Hale, M. W., O’Shea, R. D., Djouma, E., van den Buuse, M., et al. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6169 · Cited by 35 · see citing works
The Current Status of Research on Chronic Traumatic Encephalopathy
Perrine, K. R., Helcer, J., Tsiouris, A. J., Pisapia, D. J., & Stieg, P. E. (2017) · World Neurosurgery · doi:10.1016/j.wneu.2017.02.084 · Cited by 34 · see citing works
Investigating the effects of subconcussion on functional connectivity using mass-univariate and multivariate approaches
Reynolds, B. B., Stanton, A. N., Soldozy, S., Goodkin, H. P., Wintermark, M., & Druzgal, T. J. (2017) · Brain Imaging and Behavior · doi:10.1007/s11682-017-9790-z · Cited by 33 · see citing works
A Systematic Review of Positron Emission Tomography of Tau, Amyloid Beta, and Neuroinflammation in Chronic Traumatic Encephalopathy: The Evidence To Date
Lee, B. G., Leavitt, M. J., Bernick, C. B., Léger, G. C., Rabinovici, G. D., & Banks, S. J. (2018) · Journal of Neurotrauma · doi:10.1089/neu.2017.5558 · Cited by 32 · see citing works
Management of concussion in soccer
Hubertus, V., Marklund, N., & Vajkoczy, P. (2019) · Acta Neurochirurgica · doi:10.1007/s00701-019-03807-6 · Cited by 28 · see citing works
Chronic Traumatic Encephalopathy and Neurodegeneration in Contact Sports and American Football
Zuckerman, S. L., Brett, B. L., Jeckell, A. S., Yengo-Kahn, A. M., & Solomon, G. S. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-180218 · Cited by 29 · see citing works
A preliminary report of cerebral white matter microstructural changes associated with adolescent sports concussion acutely and subacutely using diffusion tensor imaging
Wu, T. C., Merkley, T. L., Wilde, E. A., Barnes, A., Li, X., Chu, Z. D., McCauley, S. R., Hunter, J. V., & Levin, H. S. (2017) · Brain Imaging and Behavior · doi:10.1007/s11682-017-9752-5 · Cited by 28 · see citing works
Head Impact Exposures Among Youth Tackle and Flag American Football Athletes
Waltzman, D., Sarmiento, K., Devine, O. J., Zhang, X., DePadilla, L., Kresnow, M., Borradaile, K. E., Hurwitz, A., Jones, D. J., Goyal, R., et al. (2021) · Sports Health A Multidisciplinary Approach · doi:10.1177/1941738121992324 · Cited by 28 · see citing works
Chronic Traumatic Encephalopathy in Athletes Involved with High-impact Sports.
Safinia, C., Bershad, E. M., Clark, H. B., SantaCruz, K. S., Alakbarova, N., Suárez, J. I., & Divani, A. A. (2016) · PubMed Central · Cited by 28 · see citing works
Interprofessional management of concussion in sport
Pabian, P. S., Oliveira, L., Tucker, J., Beato, M. C., & Gual, C. G. (2016) · Physical Therapy in Sport · doi:10.1016/j.ptsp.2016.09.006 · Cited by 27 · see citing works
Individual variations in dose response for spatial memory learning among outbred wistar rats exposed from 5 to 20 cGy of 56Fe particles
Wyrobek, A. J., & Britten, R. A. (2016) · Environmental and Molecular Mutagenesis · doi:10.1002/em.22018 · Cited by 26 · see citing works
Neurocognitive performance and mental health of retired female football players compared to non-contact sport athletes
Prien, A., Feddermann‐Demont, N., Verhagen, E. A. L. M., Twisk, J. W. R., & Junge, A. (2020) · BMJ Open Sport & Exercise Medicine · doi:10.1136/bmjsem-2020-000952 · Cited by 26 · see citing works
The multi-factorial origins of Chronic Traumatic Encephalopathy (CTE) symptomology in post-career athletes: The athlete post-career adjustment (AP-CA) model
Gaetz, M. (2017) · Medical Hypotheses · doi:10.1016/j.mehy.2017.03.023 · Cited by 26 · see citing works
Benefits of team sport participation versus concerns of chronic traumatic encephalopathy: prioritizing the health of our youth
Zuckerman, S. L., Yengo-Kahn, A. M., Brett, B. L., Kuhn, A. W., Wolfson, D. I., & Kerr, Z. Y. (2020) · Concussion · doi:10.2217/cnc-2020-0006 · Cited by 24 · see citing works
Alterations of transcriptome signatures in head trauma-related neurodegenerative disorders
Cho, H., Hyeon, S. J., Shin, J.-Y., Alvarez, V. E., Stein, T. D., Lee, J.-H., Kowall, N. W., McKee, A. C., Ryu, H., & Seo, J. (2020) · Scientific Reports · doi:10.1038/s41598-020-65916-y · Cited by 23 · see citing works
The science and questions surrounding chronic traumatic encephalopathy
Ban, V. S., Madden, C. J., Bailes, J. E., Batjer, H. H., & Lonser, R. R. (2016) · Neurosurgical FOCUS · doi:10.3171/2016.2.focus15609 · Cited by 24 · see citing works
Fluid Biomarkers for Chronic Traumatic Encephalopathy
Shahim, P., Gill, J., Blennow, K., & Zetterberg, H. (2020) · Seminars in Neurology · doi:10.1055/s-0040-1715095 · Cited by 23 · see citing works
A narrative review of psychiatric features of traumatic encephalopathy syndrome as conceptualized in the 20th century
Iverson, G. L., Kissinger-Knox, A. M., Huebschmann, N. A., Castellani, R. J., & Gardner, A. J. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1214814 · Cited by 22 · see citing works
The Effects of Blast Exposure on Protein Deimination in the Brain
Attilio, P. J., Flora, M. N., Kamnaksh, A., Bradshaw, D. V., Agoston, D. V., & Mueller, G. P. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/8398072 · Cited by 22 · see citing works
Chronic traumatic encephalopathy: fluid biomarkers
Zetterberg, H., & Blennow, K. (2018) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63954-7.00030-6 · Cited by 21 · see citing works
Interrelationships Among Neuroimaging Biomarkers, Neuropsychological Test Data, and Symptom Reporting in a Cohort of Retired National Football League Players
Kuhn, A. W., Zuckerman, S. L., Solomon, G. S., Casson, I. R., & Viano, D. C. (2016) · Sports Health A Multidisciplinary Approach · doi:10.1177/1941738116674006 · Cited by 21 · see citing works
Molecular mechanisms of chronic traumatic encephalopathy
van den Bedem, H., & Ellen Kuhl, A. (2017) · Current Opinion in Biomedical Engineering · doi:10.1016/j.cobme.2017.02.003 · Cited by 21 · see citing works
Sport related concussion – Potential for biomarkers to improve acute management
Costello, D. M., Kaye, A. H., O'Brien, T. J., & Shultz, S. R. (2018) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2018.07.002 · Cited by 19 · see citing works
No Seasonal Changes in Cognitive Functioning Among High School Football Athletes: Implementation of a Novel Electrophysiological Measure and Standard Clinical Measures
Broglio, S. P., Williams, R. M., Rettmann, A., Moore, B., Eckner, J. T., & Meehan, S. K. (2017) · Clinical Journal of Sport Medicine · doi:10.1097/jsm.0000000000000420 · Cited by 18 · see citing works
Severe Suicidality in Athletes with Chronic Traumatic Encephalopathy: A Case Series and Overview on Putative Ethiopathogenetic Mechanisms
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Authors: Iverson, G. L., Gardner, A. J., McCrory, P., Zafonte, R., & Castellani, R. J.
Affiliations: Harvard University (US)
Hunter New England Local Health District (AU)
Florey Institute of Neuroscience and Mental Health (AU)
Brigham and Women's Hospital (US)
University of Maryland, Baltimore (US)
Corresponding author: Iverson, Grant L.
ORCID: Iverson, Grant L.
Gardner, Andrew J.
McCrory, Paul
Zafonte, Ross
Castellani, Rudy J.
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2015-09
Volume: 56
Pages: 276-293
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2015.05.008
OpenAlex: W929294836
Cited by: 103
References: 228
Citations by year: 2026: 3 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 4 · 2021: 8 · 2020: 10 · 2019: 12 · 2018: 12 · 2017: 23 · 2016: 20 · 2015: 2 · 2014: 1
FWCI: 2.47
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
NOVA (University of Newcastle Australia) (submittedVersion)
Topics: Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Keywords: chronic traumatic encephalopathy, tau phosphorylation, axonal varicosities, axonal loss, TDP-43 inclusions, amyloid-beta, neurodegeneration, depression, frontotemporal dementia, behavioral symptoms, cognitive impairment, neuropathology
MeSH terms: Cognition Disorders, Dementia, DNA-Binding Proteins, Humans, tau Proteins, Disease Progression, Brain Injury, Chronic

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A critical review of chronic traumatic encephalopathy

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