The spectrum of disease in chronic traumatic encephalopathy
Open accessAbstract
Chronic traumatic encephalopathy is a progressive tauopathy that occurs as a consequence of repetitive mild traumatic brain injury. We analysed post-mortem brains obtained from a cohort of 85 subjects with histories of repetitive mild traumatic brain injury and found evidence of chronic traumatic encephalopathy in 68 subjects: all males, ranging in age from 17 to 98 years (mean 59.5 years), including 64 athletes, 21 military veterans (86% of whom were also athletes) and one individual who engaged in self-injurious head banging behaviour. Eighteen age- and gender-matched individuals without a history of repetitive mild traumatic brain injury served as control subjects. In chronic traumatic encephalopathy, the spectrum of hyperphosphorylated tau pathology ranged in severity from focal perivascular epicentres of neurofibrillary tangles in the frontal neocortex to severe tauopathy affecting widespread brain regions, including the medial temporal lobe, thereby allowing a progressive staging of pathology from stages I-IV. Multifocal axonal varicosities and axonal loss were found in deep cortex and subcortical white matter at all stages of chronic traumatic encephalopathy. TAR DNA-binding protein 43 immunoreactive inclusions and neurites were also found in 85% of cases, ranging from focal pathology in stages I-III to widespread inclusions and neurites in stage IV. Symptoms in stage I chronic traumatic encephalopathy included headache and loss of attention and concentration. Additional symptoms in stage II included depression, explosivity and short-term memory loss. In stage III, executive dysfunction and cognitive impairment were found, and in stage IV, dementia, word-finding difficulty and aggression were characteristic. Data on athletic exposure were available for 34 American football players; the stage of chronic traumatic encephalopathy correlated with increased duration of football play, survival after football and age at death. Chronic traumatic encephalopathy was the sole diagnosis in 43 cases (63%); eight were also diagnosed with motor neuron disease (12%), seven with Alzheimer's disease (11%), 11 with Lewy body disease (16%) and four with frontotemporal lobar degeneration (6%). There is an ordered and predictable progression of hyperphosphorylated tau abnormalities through the nervous system in chronic traumatic encephalopathy that occurs in conjunction with widespread axonal disruption and loss. The frequent association of chronic traumatic encephalopathy with other neurodegenerative disorders suggests that repetitive brain trauma and hyperphosphorylated tau protein deposition promote the accumulation of other abnormally aggregated proteins including TAR DNA-binding protein 43, amyloid beta protein and alpha-synuclein.
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Prior to 2015, there were no agreed upon neuropathological criteria for CTE, and the criteria put forward by the two research groups in the US differed.
“Prior to 2015, there were no agreed upon neuropathological criteria for CTE, and the criteria put forward by the two research groups in the US differed [15, 16].”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [16]
The 'Definition of chronic traumatic encephalopathy' section sets out this research group's neuropathological criteria for CTE. Our copy does not say that agreed neuropathological criteria were lacking before 2015 or compare criteria proposed by two US research groups. Its statement that clinical criteria needed to be established concerns a different kind of criteria. (LLM, conf=0.76)
Experimental — accuracy not yet measuredIt is well established that a large percentage of former athletes identified as having CTE neuropathology also have neuropathology associated with age related neurodegenerative diseases such as AD, PD, Lewy body disease, hippocampal sclerosis, and ALS to the extent that they meet full neuropathological criteria for an alternative, well-characterized neurodegenerative disease.
“It is now well established that a large percentage of former athletes identified as having CTE neuropathology also have neuropathology associated with age related neurodegenerative diseases such as AD, PD, Lewy body disease, hippocampal sclerosis, and ALS [14, 41–44] to the extent that they meet full neuropathological criteria for an alternative, well-characterized neurodegenerative disease [16].”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [16]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredOver the past decade, the clinical features attributed to CTE have been expanded greatly and include virtually any mental health or neurological symptom or problem present prior to death.
“Over the past decade, the clinical features attributed to CTE have been expanded greatly and include virtually any mental health or neurological symptom or problem present prior to death”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [16]
The Introduction and Clinical symptoms section associate CTE with a wide range of psychiatric, cognitive and neurological symptoms. They do not say that the list expanded greatly over the past decade or that virtually any symptom present before death is attributed to CTE. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe compact NFTs observed are morphologically most like those seen in primary age-related tauopathy (PART), Alzheimer's disease (AD), and chronic traumatic encephalopathy (CTE), but the topographical distribution and immunostaining characteristics differ from these more common tauopathies.
“The compact NFTs observed are morphologically most like those seen in primary age-related tauopathy (PART) [4], Alzheimer’s disease (AD) [22], and chronic traumatic encephalopathy (CTE) [13, 14], but the topographical distribution and immunostaining characteristics differ from these more common tauopathies in several respects.”
From Tuberous sclerosis complex is associated with a novel human tauopathy (2023) · cites this paper as [14]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredPART, AD, and CTE all show a balanced 3R/4R tauopathy, prominent neuropil threads, and ready detection with CP13, MC1, and p62 antibodies.
“Finally, PART, AD, and CTE all show a balanced 3R/4R tauopathy, prominent neuropil threads, and ready detection with CP13, MC1, and p62 antibodies [14, 20, 24]”
From Tuberous sclerosis complex is associated with a novel human tauopathy (2023) · cites this paper as [14]
The Neuropathology of chronic traumatic encephalopathy section reports that CTE tangles stain for both 3R and 4R tau, and Figure 1 describes CP-13-positive neuropil threads in CTE. It does not establish a balanced 3R/4R ratio or detection with MC1 and p62; the paper also does not address PART. Its comparison table discusses 3R and 4R tau in AD, but does not establish the full set of shared features claimed for all three conditions. (LLM, conf=0.88)
Experimental — accuracy not yet measured
The consensus panel did not adopt the four neuropathological phenotypes or stages of CTE, and indicated that the preliminary criteria were a first step along the path to standardizing the neuropathology of CTE.
“The consensus panel did not adopt the four neuropathological phenotypes [15] or stages of CTE [16], and indicated that the preliminary criteria were a “first step along the path to standardizing the neuropathology of CTE” [30].”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [16]
Noy et al. identified CTE pathology, based on the staging system of McKee et al., in 4.5% (three cases of Stage I and two cases of Stage II).
“They identified CTE pathology, based on the staging system of McKee et al. [16], in 4.5% (three cases of Stage I and two cases of Stage II).”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [16]
It is well established that some people who have large exposures to repetitive neurotrauma, such as retired professional football players or boxers, had only Stage I or Stage II CTE at the time of their deaths, and some of these individuals died in their 80s.
“It is well established that some people who have large exposures to repetitive neurotrauma, such as retired professional football players or boxers, had only Stage I or Stage II CTE at the time of their deaths [16], and some of these individuals died in their 80s.”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [16]
In the Ling et al. UK study, all cases were considered Stage I or Stage II based on McKee staging, and their mean age of death was 81.0 years.
“All cases were considered Stage I or Stage II based on the staging system of McKee and colleagues [16], and their mean age of death was 81.0 years.”
From The Need to Separate Chronic Traumatic Encephalopathy Neuropathology from Clinical Features (2017) · cites this paper as [16]
CTE stage (I to IV) is based on extent and severity of ptau pathology.
“The stage of CTE (I to IV) is based on the extent and severity of ptau pathology (8).”
From Chronic Traumatic Encephalopathy Within an Amyotrophic Lateral Sclerosis Brain Bank Cohort (2018) · cites this paper as [8]
Prior to 2016, there were no agreed upon neuropathological criteria for CTE, and the criteria published by the 2 leading research groups in the United States differed substantially.
“Prior to 2016, there were no agreed upon neuropathological criteria for CTE, and the criteria published by the 2 leading research groups in the United States differed substantially (7,14).”
From Mild Chronic Traumatic Encephalopathy Neuropathology in People With No Known Participation in Contact Sports or History of Repetitive Neurotrauma (2019) · cites this paper as [14]
Noy et al identified 4.5% of their cases as having CTE (3 cases of Stage I and 2 cases of Stage II).
“They attempted to use the staging system of McKee et al (14), and they identified 4.5% of their cases as having CTE (3 cases of Stage I and 2 cases of Stage II).”
From Mild Chronic Traumatic Encephalopathy Neuropathology in People With No Known Participation in Contact Sports or History of Repetitive Neurotrauma (2019) · cites this paper as [14]
NFTs in CTE differ from AD in topography, and individual NFTs in CTE are generally larger with more dot-like and spindle-shaped neurites.
“In addition to a different topography of NFTs in CTE compared to AD, the size of individual NFTs in CTE is generally larger and the neurites are more dot like and spindle shaped [128].”
From The neuropathology of sport (2014) · cites this paper as [128]
CTE is similar to AD in its tau isoform profile and phosphorylation state, and neuronal tau pathology is immunoreactive to both 3R and 4R tau.
“CTE is similar to AD in its tau isoform profile and phosphorylation state [165], and neuronal tau pathology is immunoreactive to both 3R and 4R tau [128].”
From The neuropathology of sport (2014) · cites this paper as [128]
Stage III CTE is characterized by reduced brain weight, mild frontal and temporal atrophy, enlargement of lateral and third ventricles, septal abnormalities in 50%, pallor of locus coeruleus and substantia nigra, atrophy of mammillary bodies, thalamus and hypothalamus, thinning of corpus callosum, and widespread NFTs including in hippocampus, entorhinal cortex, amygdala, nucleus basalis of Meynert
“In Stage III CTE, most brains show reduced brain weight, mild frontal and temporal atrophy, and enlargement of the lateral and third ventricles. Septal abnormalities are common (50 %), including cavum septum pellucidum or septal fenestrations. There is often pallor of the locus coeruleus and substantia nigra, atrophy of the mammillary bodies, thalamus and hypothalamus, and thinning of the corpus”
From The neuropathology of sport (2014) · cites this paper as [128]
Axonal pathology is present at all stages of CTE and becomes more severe as CTE stage advances.
“In addition to PHF-tau pathology, axonal pathology is present at all stages of CTE and becomes more severe as CTE stage advances [72, 128].”
From The neuropathology of sport (2014) · cites this paper as [128]
Despite evidence for Ab deposition in moderate to severe TBI, Ab plaques have not been found in early or mild stages of CTE in young individuals, but occur in older subjects with CTE in association with increased age at death.
“However, despite evidence for Ab deposition in moderate to severe TBI [94], Ab plaques have not been found in early or mild stages of CTE in young individuals [65, 66, 72, 91, 126] but occur in older subjects with CTE in association with increased age at death [128].”
From The neuropathology of sport (2014) · cites this paper as [128]
Stage II CTE is characterized by multiple foci of PHF-tau pathology at the depths of sulci, commonly in frontal, temporal, parietal, insular, and septal cortices; NFTs in superficial layers of adjacent cerebral cortex, locus coeruleus, and substantia innominata, with medial temporal lobe structures spared; mild neurofibrillary degeneration in deep structures; and rare TDP-43 neuropil threads and
“Microscopically, multiple foci of PHF-tau pathology are found at the depths of the sulci, commonly in the frontal, temporal, parietal, insular, and septal cortices (Figs. 2, 3, 6). NFTs are also found in superficial layers of the adjacent cerebral cortex, locus coeruleus and substantia innominata, but the medial temporal lobe structures are spared. Deep structures such as the substantia nigra, dor”
From The neuropathology of sport (2014) · cites this paper as [128]
Ab deposition is found in 13% of Stage III CTE cases as sparse diffuse and neuritic Ab plaques and vascular amyloid.
“Ab deposition is found in 13 % of cases as sparse diffuse and neuritic Ab plaques and vascular amyloid.”
From The neuropathology of sport (2014) · cites this paper as [128]
The majority of Stage III CTE cases show TDP-43-positive neurites and inclusions in cerebral cortex, medial temporal lobe, diencephalon, and brainstem.
“The majority of cases show TDP-43-positive neurites and inclusions in cerebral cortex, medial temporal lobe, diencephalon, and brainstem.”
From The neuropathology of sport (2014) · cites this paper as [128]
Stage I CTE is characterized by one or two isolated perivascular foci of PHF-tau NFTs and dot-like neuropil threads, most commonly at the depths of cerebral sulci of the frontal cortex, usually with subpial PHF-tau positive astrocytes; NFTs are also commonly found in the locus coeruleus; about half of Stage I cases have abnormal TDP-43 inclusions within subcortical frontal white matter and fornix;
“Microscopically, there are one or two isolated perivascular foci of PHF-tau NFTs and dot-like neuropil threads, most commonly found at the depths of cerebral sulci of the frontal cortex (Fig. 2) and usually in association with subpial PHF-tau positive astrocytes. NFTs are also commonly found in the locus coeruleus. About half of Stage I cases will also have abnormal TDP-43 inclusions within the s”
From The neuropathology of sport (2014) · cites this paper as [128]
Abnormal TDP-43 pathology is found in all stages of CTE; in early stages the inclusions consist of neuritic threads and dot-like inclusions in subpial, perivascular, and periventricular regions; cytoplasmic neuronal inclusions are first seen in Stage II disease and are characteristic of late stages where they partially co-localize with PHF-tau inclusions.
“Abnormal TDP-43 pathology is found in all stages of CTE. In early stages the inclusions consist of neuritic threads and dot-like inclusions in subpial, perivascular, and periventricular regions; cytoplasmic neuronal inclusions are first seen in Stage II disease and are characteristic of late stages where they partially co-localize with PHF-tau inclusions [128].”
From The neuropathology of sport (2014) · cites this paper as [128]
Provisional criteria for the pathological diagnosis of CTE and four pathological stages of severity have been proposed based on the topography of PHF-tau pathology.
“Provisional criteria for the pathological diagnosis of CTE and four pathological stages of severity have been proposed based on the topography of PHF-tau pathology [128]; formal consensus validation of these diagnostic and staging criteria by a large group of neuropathologists is currently in progress”
From The neuropathology of sport (2014) · cites this paper as [128]
Stage IV CTE is characterized by significant reduction of brain weight, pronounced atrophy of frontal and temporal lobes, medial temporal lobe, and anterior thalamus, marked enlargement of lateral and third ventricles, severe spongiosus of layer 2, widespread neuronal loss, severe PHF-tau deposition, and severe widespread TDP-43 deposition.
“Brains with Stage IV CTE usually show significant reduction of brain weight (Fig. 4), with pronounced atrophy of the frontal and temporal lobes, medial temporal lobe, and anterior thalamus. The hypothalamic floor is thinned, the mammillary bodies are darkly discolored and atrophied, and there is marked enlargement of the lateral and third ventricles.”
From The neuropathology of sport (2014) · cites this paper as [128]
CTE has been diagnosed neuropathologically in American football players, professional and amateur boxers, ice hockey players, professional wrestlers, soccer players, rugby players, and a professional baseball player.
“Although CTE was first identified in association with boxing, CTE has been diagnosed neuropathologically in American football players, professional and amateur boxers, ice hockey players, professional wrestlers, soccer players, rugby players, and a professional baseball player (Figs. 3, 4, 5, 6) [38, 65, 66, 88, 91, 127, 128, 146–148].”
From The neuropathology of sport (2014) · cites this paper as [128]
In our current experience of 103 neuropathologically confirmed cases of CTE, there have been 13 individuals who developed a progressive motor neuron disease (MND) (13%).
“In our current experience of 103 neuropathologically confirmed cases of CTE, there have been 13 individuals who developed a progressive motor neuron disease (MND) (13 %) [128].”
From The neuropathology of sport (2014) · cites this paper as [128]
In different autopsy series, the percentage of former professional American football players who have died and donated their brains to research varies from 50%, 80%, to 97%.
“In different autopsy series, the percentage of former professional American football players who have died and donated their brains to research varies from 50 % [88], 80 % [146], to 97 %) [128].”
From The neuropathology of sport (2014) · cites this paper as [128]
In all cases of CTE-MND, there is a distinct TDP-43 proteinopathy affecting the brain and spinal cord.
“In all cases, there is a distinct TDP-43 proteinopathy affecting the brain and spinal cord (Fig. 6) [128].”
From The neuropathology of sport (2014) · cites this paper as [128]
CTE is associated with the development of other neurodegenerations, notably Lewy body disease, AD, frontotemporal lobar degeneration, and motor neuron disease.
“CTE is associated with the development of other neurode-generations, notably Lewy body disease (LBD), AD, fron-totemporal lobar degeneration (FTLD), and motor neuron disease (MND) [127, 128].”
From The neuropathology of sport (2014) · cites this paper as [128]
Either repetitive trauma or the accumulation of tau pathology in CTE provokes the deposition of other abnormal proteins involved in neurodegeneration.
“In our current experience of 103 neuropathologically confirmed cases of CTE, co-existent LBD was found in 12 (12 %) cases, MND in 13 (13 %), AD in 15 (15 %), and FTLD in 6 (6 %), suggesting that either repetitive trauma or the accumulation of tau pathology in CTE provokes the deposition of other abnormal proteins involved in neurodegeneration [127, 128].”
From The neuropathology of sport (2014) · cites this paper as [128]
In our current experience of 103 neuropathologically confirmed cases of CTE, co-existent LBD was found in 12 (12%) cases, MND in 13 (13%), AD in 15 (15%), and FTLD in 6 (6%).
“In our current experience of 103 neuropathologically confirmed cases of CTE, co-existent LBD was found in 12 (12 %) cases, MND in 13 (13 %), AD in 15 (15 %), and FTLD in 6 (6 %), suggesting that either repetitive trauma or the accumulation of tau pathology in CTE provokes the deposition of other abnormal proteins involved in neurodegeneration [127, 128].”
From The neuropathology of sport (2014) · cites this paper as [128]
Among American football players, the stage of CTE at death significantly correlates with age at death, number of years playing football, and number of years after retirement from football.
“Among American football players, the stage of CTE at death significantly correlates with age at death, number of years playing football, and number of years after retirement from football [128].”
From The neuropathology of sport (2014) · cites this paper as [128]
The progression of CTE from a multifocal state (Stage II) to widespread disease (Stage III) might represent a period of exponential increase in PHF-tau accumulation, hypothetically from such mechanisms as protein templating or other modes of interneuronal spreading.
“The progression of CTE from a multifocal state (Stage II) to widespread disease (Stage III) might represent a period of exponential increase in PHF-tau accumulation, hypothetically from such mechanisms as protein templating or other modes of interneuronal spreading [128].”
From The neuropathology of sport (2014) · cites this paper as [128]
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“On the other hand, tau pathology, including neuronal and astroglial, in CTE is more abundant in the depths of the convexity cerebral sulci, especially in early stages [41], an aspect that has not been reported in tau astrogliopathy in the aging brain [29, 34-36, 46, 57].”
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“All cases were considered Stage I or Stage II based on the staging system of McKee and colleagues [16], and their mean age of death was 81.”
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- Authors
- McKee, A. C., Stein, T. D., Nowinski, C. J., Stern, R. A., Daneshvar, D. H., Alvarez, V. E., Lee, H.-S., Hall, G., Wojtowicz, S. M., Baugh, C. M., Riley, D. O., Kubilus, C. A., Cormier, K. A., Jacobs, M. A., Martin, B. R., Abraham, C. R., Ikezu, T., Reichard, R. R., Wolozin, B. L., Budson, A. E., Goldstein, L. E., Kowall, N. W., & Cantu, R. C.
- Affiliations
- United States Department of Veterans Affairs (US)
- Boston University (US)
- University of Massachusetts Lowell (US)
- Mayo Clinic (US)
- ORCID
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-12-02
- Volume
- 136
- Issue
- 1
- Pages
- 43-64
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC3624697
- OpenAlex
- W2141679195
- Cited by
- 2,098
- References
- 85
- Citations by year
- 2026: 84 · 2025: 117 · 2024: 116 · 2023: 123 · 2022: 133 · 2021: 168 · 2020: 204 · 2019: 196 · 2018: 176 · 2017: 172 · 2016: 176 · 2015: 172 · 2014: 149 · 2013: 104 · 2012: 1
- FWCI
- 101.18
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Brain (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Veterans Affairs (B6796-C, I01 CX001038, AG13846, P30 AG13846, CSP501)
- National Operating Committee on Standards for Athletic Equipment
- Traumatic Brain Injury Center of Excellence
- National Institute on Aging (R01AG1649, P30AG013846)
- National Institute of Neurological Disorders and Stroke (R56NS078337, R21NS066108, R21NS073679, R01NS078337, R01NS060872)
- National Institute of Environmental Health Sciences (R01ES020395)
- National Institute of Child Health and Human Development
- Topics
- Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
- Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- chronic traumatic encephalopathy, repetitive mild traumatic brain injury, hyperphosphorylated tau, neurofibrillary tangles, axonal varicosities, axonal loss, TDP-43 inclusions, cognitive impairment, dementia, motor neuron disease, Alzheimer's disease, Lewy body disease, frontotemporal lobar degeneration, American football players, military veterans
- MeSH terms
- Adolescent, Adult, Aged, Aged, 80 and over, Brain, Football, Humans, Male, Middle Aged, Veterans, Neurofibrillary Tangles, tau Proteins, Disease Progression, Brain Injury, Chronic, Tauopathies, Athletes
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