Neurofibrillary tangle pathology and Braak staging in chronic epilepsy in relation to traumatic brain injury and hippocampal sclerosis: a post-mortem study.
Open accessAbstract
The long-term pathological effects of chronic epilepsy on normal brain ageing are unknown. Previous clinical and epidemiological studies show progressive cognitive decline in subsets of patients and an increased prevalence of Alzheimer's disease in epilepsy. In a post-mortem series of 138 patients with long-term, mainly drug-resistant epilepsy, we carried out Braak staging for Alzheimer's disease neurofibrillary pathology using tau protein immunohistochemistry. The stages were compared with clinicopathological factors, including seizure history and presence of old traumatic brain injury. Overall, 31% of cases were Braak Stage 0, 36% Stage I/II, 31% Stage III/IV and 2% Stage V/VI. The mean age at death was 56.5 years and correlated with Braak stage (P < 0.001). Analysis of Braak stages within age groups showed a significant increase in mid-Braak stages (III/IV), in middle age (40-65 years) compared with data from an ageing non-epilepsy series (P < 0.01). There was no clear relationship between seizure type (generalized or complex partial), seizure frequency, age of onset and duration of epilepsy with Braak stage although higher Braak stages were noted with focal more than with generalized epilepsy syndromes (P < 0.01). In 30% of patients, there was pathological evidence of traumatic brain injury that was significantly associated with higher Braak stages (P < 0.001). Cerebrovascular disease present in 40.3% and cortical malformations in 11.3% were not significantly associated with Braak stage. Astrocytic-tau protein correlated with the presence of both traumatic brain injury (P < 0.01) and high Braak stage (P < 0.001). Hippocampal sclerosis, identified in 40% (bilateral in 48%), was not associated with higher Braak stages, but asymmetrical patterns of tau protein accumulation within the sclerotic hippocampus were noted. In over half of patients with cognitive decline, the Braak stage was low indicating causes other than Alzheimer's disease pathology. In summary, there is evidence of accelerated brain ageing in severe chronic epilepsy although progression to high Braak stages was infrequent. Traumatic brain injury, but not seizures, was associated with tau protein accumulation in this series. It is likely that Alzheimer's disease pathology is not the sole explanation for cognitive decline associated with epilepsy.
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P-tau pathology is found in patients with temporal lobe epilepsy, Dravet syndrome, Nodding syndrome, Niemann-Pick type C disease, focal cortical dysplasia IIB, and tuberous sclerosis complex, as well as animal models of post-traumatic epilepsy, Lafora disease, and autism spectrum disorder.
“These include patients with TLE, Dravet syndrome, Nodding syndrome (Thom et al., 2011; Pollanen et al., 2018; Hotterbeekx et al., 2019), Niemann-Pick type C disease (NPC) (Auer et al., 1995; Love et al., 1995; Suzuki et al., 1995; Malnar et al., 2014), focal cortical dysplasia IIB (FCDIIb) (Sen et al., 2007; Iyer et al., 2014), and tuberous sclerosis complex (TSC) (Sarnat and Flores-Sarnat, 2015;”
From Tauopathy and Epilepsy Comorbidities and Underlying Mechanisms (2022) · cites this paper as Thom et al., 2011
The Results report AT8-positive astrocytes in the chronic-epilepsy series and neurofibrillary tangles in some cortical malformations, supporting p-tau pathology in some patients with epilepsy. But the Discussion says the three patients with Dravet syndrome had no neuropathological or degenerative changes; this paper therefore does not support the Dravet part of the cited group. No page numbers are available in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIncreased levels of p-tau in the brain are found across many seizure disorders.
“While levels of endogenous or total tau differ across examinations of patients with epilepsy, increased levels of p-tau in the brain are found across many seizure disorders (Thom et al., 2011).”
From Tauopathy and Epilepsy Comorbidities and Underlying Mechanisms (2022) · cites this paper as Thom et al., 2011
The Discussion (page not provided) reports age-accelerated tau accumulation in a post-mortem series of patients with mainly long histories of drug-resistant epilepsy. That supports abnormal brain tau pathology in this group, but not increased p-tau levels across many seizure disorders. The Abstract (page not provided) also says traumatic brain injury, rather than seizures, was associated with tau accumulation in this series. (LLM, conf=0.85)
Experimental — accuracy not yet measuredIn a post-mortem series of 138 refractory epilepsy cases, Braak staging of neurofibrillary tangles in the age group 40-65 years revealed increased Braak stages III/IV compared with age-matched non-epilepsy cases.
“In a post-mortem series of 138 refractory epilepsy cases of diverse causes, Braak staging of NFTs in the age group 40–65 years revealed increased Braak stages III/IV compared with data from an age-matched series of non-epilepsy cases (Thom et al., 2011).”
From Tauopathy and Epilepsy Comorbidities and Underlying Mechanisms (2022) · cites this paper as Thom et al., 2011
Tau pathology is not universally found in connection with epileptic activity.
“It should also be noted that tau pathology is not universally found in connection with epileptic activity.”
From Tauopathy and Epilepsy Comorbidities and Underlying Mechanisms (2022) · cites this paper as Thom et al., 2011
31% of the post-mortem refractory epilepsy cases studied by Thom et al. (2011) were classified as Braak Stage 0.
“For instance, 31% of the post-mortem refractory epilepsy cases studied by Thom et al. (2011) were classified as Braak Stage 0, and analysis of surgically resected tissue from 56 TLE patients by Silva et al. (2021) found p-tau-positive neurons in only two samples.”
From Tauopathy and Epilepsy Comorbidities and Underlying Mechanisms (2022) · cites this paper as Thom et al., 2011
In humans with chronic epilepsy, elevated p-tau is present in post-mortem as well as surgically resected tissue.
“And in humans with chronic epilepsy, elevated p-tau is present in post-mortem (Thom et al., 2011) as well as surgically resected tissue (Puvenna et al., 2016; Tai et al., 2016; Liu C. et al., 2017; Prada Jardim et al., 2018; Smith et al., 2019; Gourmaud et al., 2020).”
From Tauopathy and Epilepsy Comorbidities and Underlying Mechanisms (2022) · cites this paper as Thom et al., 2011
Post-mortem analysis of 138 refractory epilepsy cases revealed that 77% of patients with Braak staging III or higher exhibited progressive cognitive decline.
“Post-mortem analysis of 138 refractory epilepsy cases revealed that 77% of patients with Braak staging III or higher exhibited progressive cognitive decline (Thom et al., 2011), and increased total and p-tau levels measured in surgically resected tissue from TLE patients are inversely correlated with cognitive scores (Kandratavicius et al., 2013; Tai et al., 2016; Gourmaud et al., 2020).”
From Tauopathy and Epilepsy Comorbidities and Underlying Mechanisms (2022) · cites this paper as Thom et al., 2011
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- Authors
- Thom, M., Liu, J. Y. W., Thompson, P., Phadke, R., Narkiewicz, M., Martinian, L., Marsdon, D., Koepp, M., Caboclo, L., Catarino, C. B., & Sisodiya, S. M.
- Affiliations
- National Hospital for Neurology and Neurosurgery (GB)
- Corresponding author
- Thom, Maria
- ORCID
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-09-08
- Volume
- 134
- Issue
- 10
- Pages
- 2969-2981
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC3187539
- OpenAlex
- W2128008503
- Cited by
- 167
- References
- 8
- Citations by year
- 2026: 12 · 2025: 12 · 2024: 18 · 2023: 15 · 2022: 15 · 2021: 15 · 2020: 8 · 2019: 10 · 2018: 14 · 2017: 11 · 2016: 10 · 2015: 9 · 2014: 5 · 2013: 5 · 2012: 8
- FWCI
- 3.96
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Brain (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- National Institute for Health and Care Research (0600934)
- University College London Hospitals NHS Foundation Trust
- Medical Research Council (0600934)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- chronic epilepsy, drug-resistant epilepsy, neurofibrillary tangles, Braak staging, tau protein, traumatic brain injury, hippocampal sclerosis, Alzheimer's disease, cognitive decline, cerebrovascular disease, malformations of cortical development, seizure types, postmortem neuropathology, age at death, seizure frequency
- MeSH terms
- Adolescent, Adult, Aged, Aged, 80 and over, Astrocytes, Brain Injuries, Epilepsy, Female, Hippocampus, Humans, Male, Middle Aged, Sclerosis, Neurofibrillary Tangles, tau Proteins, Disease Progression
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