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Chronic traumatic encephalopathy and aging-related tau astrogliopathy in community-dwelling older persons with and without moderate-to-severe traumatic brain injury.

ABSTRACT: This study examined the frequency of chronic traumatic encephalopathy-neuropathologic change (CTE-NC) and aging-related tau astrogliopathy (ARTAG) in community-dwelling older adults and tested the hypothesis that these tau pathologies are associated with a history of moderate-to-severe traumatic brain injury (msTBI), defined as a TBI with loss of consciousness >30 minutes. We evaluated CTE-NC, ARTAG, and Alzheimer disease pathologies in 94 participants with msTBI and 94 participants without TBI matched by age, sex, education, and dementia status TBI from the Rush community-based cohorts. Six (3%) of brains showed the pathognomonic lesion of CTE-NC; only 3 of these had a history of msTBI. In contrast, ARTAG was common in older brains (gray matter ARTAG = 77%; white matter ARTAG = 54%; subpial ARTAG = 51%); there were no differences in severity, type, or distribution of ARTAG pathology with respect to history of msTBI. Furthermore, those with msTBI did not have higher levels of PHF-tau tangles density but had higher levels of amyloid-β load (Estimate = 0.339, SE = 0.164, p = 0.040). These findings suggest that CTE-NC is infrequent while ARTAG is common in the community and that both pathologies are unrelated to msTBI. The association of msTBI with amyloid-β, rather than with tauopathies suggests differential mechanisms of neurodegeneration in msTBI.

SUBMITTER: Agrawal S

PROVIDER: S-EPMC10880068 | biostudies-literature | 2024 Feb

REPOSITORIES: biostudies-literature

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Chronic traumatic encephalopathy and aging-related tau astrogliopathy in community-dwelling older persons with and without moderate-to-severe traumatic brain injury.

Agrawal Sonal S Leurgans Sue E SE Barnes Lisa L LL Dams-O'Connor Kristen K Mez Jesse J Bennett David A DA Schneider Julie A JA

Journal of neuropathology and experimental neurology 20240201 3

This study examined the frequency of chronic traumatic encephalopathy-neuropathologic change (CTE-NC) and aging-related tau astrogliopathy (ARTAG) in community-dwelling older adults and tested the hypothesis that these tau pathologies are associated with a history of moderate-to-severe traumatic brain injury (msTBI), defined as a TBI with loss of consciousness >30 minutes. We evaluated CTE-NC, ARTAG, and Alzheimer disease pathologies in 94 participants with msTBI and 94 participants without TBI ...[more]

PMID: 38300796

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Project description:Background and objectivesThe consensus criteria for traumatic encephalopathy syndrome (TES), the possible in vivo clinical syndrome associated with significant repetitive head impacts, have only been minimally studied to date. This study examined the prevalence of the proposed core clinical features of TES in a sample of healthy adults.MethodsA cross-sectional survey study was conducted through ResearchMatch, a national health volunteer registry. Participants were assessed for symptoms of TES based on the 2021 consensus criteria, including prior repetitive head impacts and core clinical features. Additional health information (e.g., concussion history, psychological health, sleep, chronic pain) was also evaluated. The consensus proposed research criteria for TES (i.e., reporting at least one progressive core clinical feature of TES, as in progressive difficulties with episodic memory, executive functioning, or neurobehavioral dysregulation) were applied to the sample.ResultsOut of 1100 participants (average age = 53.6 ± 17.7 years, 55% women), 34.6% endorsed one or more progressive core clinical features of TES. Participants with a significant history of contact sports (i.e., ≥ 5 years total, with ≥ 2 years in high school or beyond) had similar rates of endorsing a progressive core clinical feature of TES compared to those without significant histories of repetitive head impacts (36.4% vs 32.8%, respectively, χ2 = 0.52, p = 0.47). A significant history of repetitive head impacts in sports was not associated with endorsing a core clinical feature of TES in univariable or multivariable models (p > 0.47), whereas current depression/anxiety (odds ratio [OR] = 6.94), a history of psychiatric disorders (OR = 2.57), current sleep problems (OR = 1.56), and younger age (OR = 0.99) were significant predictors of TES status in a multivariable model. In a subsample of 541 participants who denied a lifetime history of contact sports, other forms of repetitive head impacts, and concussions, approximately 31.0% endorsed one or more progressive core clinical features of TES. Additionally, 73.5% of neurotrauma-naïve participants with current anxiety or depression reported at least one core progressive feature of TES, compared with 20.2% of those without clinically significant depression/anxiety symptoms.ConclusionsA considerable proportion of adults without a significant history of repetitive head impacts from sports endorsed core TES features, particularly those experiencing mental health symptoms. Having a significant history of contact sports was not associated with endorsing a core progressive clinical feature of TES, whereas other health factors were. These findings underscore the need for validating and refining TES criteria in samples with and without substantial neurotrauma histories.

Project description:ImportanceA history of traumatic brain injury (TBI) has been considered a risk factor for Alzheimer dementia. However, the specific association of TBI, even without loss of consciousness (LOC), with pathologic findings that underlie Alzheimer dementia, including Alzheimer disease (AD), non-AD neurodegenerative, and vascular pathologic findings, remains unclear.ObjectiveTo examine the association between TBI with and without LOC and neuropathologic findings in community-based cohorts.Design, setting, and participantsThis cross-sectional analysis used neuropathologic data from 1689 participants from the Religious Orders Study, the Rush Memory and Aging Project, and the Minority Aging Research Study. These studies began enrollment in 1994, 1997, and 2004, respectively. The current study's data set was frozen on April 3, 2021, when the mean (SD) length of follow-up for the participants was 8.7 (5.5) years.ExposureTraumatic brain injury exposure was assessed using a standardized, self-reported questionnaire at baseline and annual follow-up visits. Participants were categorized into those (1) without TBI exposure (n = 1024), (2) with TBI with LOC (n = 161), or (3) with TBI without LOC (n = 504).Main outcomes and measuresNeuropathologic measures of amyloid-β, paired helical filament tangles, neocortical Lewy bodies, transactive response DNA-binding protein 43, hippocampal sclerosis, gross infarcts, and microinfarcts were assessed. Multiple linear regression and logistic regression models were used to determine whether TBI with or without LOC (compared with no TBI exposure as the reference group) was associated with neuropathologic outcomes after adjusting for age at death, sex, and educational level. Whether the apolipoprotein E (APOE) ε4 allele and sex differences modified associations was also examined.ResultsA total of 1689 participants (1138 [67%] women and 551 [33%] men; mean [SD] age at death, 89.2 [6.7] years; 80 [5%] Black, 46 [3%] Latino, 1639 [97%] non-Latino, and 1601 [95%] White) participated in the study. Compared with participants without TBI, participants with TBI with LOC had a greater amyloid-β load (estimate, 0.25; 95% CI, 0.06-0.43; P = .008) and higher odds of having 1 or more gross infarcts (odds ratio [OR], 1.45; 95% CI, 1.04-2.02; P = .02) and 1 or more microinfarcts (OR, 1.70; 95% CI, 1.21-2.38; P = .002), particularly subcortical microinfarcts (OR, 1.85; 95% CI, 1.23-2.79; P = .002). Those with TBI without LOC had higher odds of neocortical Lewy bodies (OR, 1.37; 95% CI, 1.01-1.87; P = .04) and 1 or more cortical microinfarcts (OR, 1.43; 95% CI, 1.09-1.87; P = .008). The association of TBI with and without LOC with vascular pathologic outcomes persisted after controlling for vascular risk factors and vascular disease burden. Traumatic brain injury with or without LOC was not associated with paired helical filament tangles, transactive response DNA-binding protein 43, or hippocampal sclerosis. No interactions occurred with APOE ε4 or sex.Conclusions and relevanceThis cross-sectional analysis suggests that a history of TBI, even without LOC, is associated with age-related neuropathologic outcomes, both neurodegenerative and vascular. The variation in the neuropathologic outcomes in individuals with and without LOC may provide clues to potential mechanisms, diagnoses, and management in persons with TBI.

Dataset Information

Chronic traumatic encephalopathy and aging-related tau astrogliopathy in community-dwelling older persons with and without moderate-to-severe traumatic brain injury.

Publications

Chronic traumatic encephalopathy and aging-related tau astrogliopathy in community-dwelling older persons with and without moderate-to-severe traumatic brain injury.

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