The prevalence of chronic traumatic encephalopathy in a historical epilepsy post-mortem collection

Ryniejska, M., El-Hachami, H., Mrzyglod, A., Liu, J.Y.W. and Thom, M. 2024. The prevalence of chronic traumatic encephalopathy in a historical epilepsy post-mortem collection. Brain Pathology. Advanced online publication. https://doi.org/10.1111/bpa.13317

TitleThe prevalence of chronic traumatic encephalopathy in a historical epilepsy post-mortem collection
TypeJournal article
AuthorsRyniejska, M., El-Hachami, H., Mrzyglod, A., Liu, J.Y.W. and Thom, M.
Abstract

Previous post-mortem epilepsy series showed phosphorylated-tau (pTau) accumulation in relation to traumatic brain injury (TBI) rather than driven by seizure frequency. The Corsellis Epilepsy Collection, established in the mid-20th century, represents brain samples collected from patients living with a range of epilepsies from the 1880’s to 1990s. Our aim was to interrogate this historical archive to explore relationships between epilepsy, trauma and tau pathology. AT8 immunohistochemistry for pTau was carried out in 102 cases (55% male, with mean age at death of 62 years) on frontal, temporal, amygdala, hippocampal and lesional cortical regions and evaluated using current NINDS criteria for chronic traumatic encephalopathy (CTE) and Braak staging with beta-amyloid, AT8-GFAP and other pTau markers (CP13, PHF1, AT100, AT180) in selected cases. CTE pathology was identified in 15.7% and associated with astroglial tau, a younger age of onset of epilepsy, evidence of TBI and institutionalisation for epilepsy compared to cases without CTE, but not for seizure type or frequency; memory impairment was noted in 43% of CTE, a significantly younger age of death and more frequent sudden and unexpected death (p<0.05-0.001). In contrast, a higher Braak stage was associated with late onset epilepsy and cognitive decline. Other pTau patterns observed were not typical for Braak or CTE stages and may represent epilepsy- related activity driving pTau accumulation. Of note, 9% of cases showed no pTau, including cases with long epilepsy duration, poor seizure control and a history of prior TBI. In summary, this cohort includes patients with more severe forms of epilepsy and CTE prevalence was more frequent than reported in non-epilepsy community-based studies (0-8%) but lower than published series from contact sports participants (32-87%). Of note pTau pathology was negative in a proportion of epilepsy cases requiring further investigation of underlying neuroprotective factors in this group.

KeywordsChronic traumatic encephalopathy
Epilepsy
Astrocytopathy
JournalBrain Pathology
ISSN1015-6305
1750-3639
Year2024
PublisherWiley
Publisher's version
License
CC BY 4.0
File Access Level
Open (open metadata and files)
Digital Object Identifier (DOI)https://doi.org/10.1111/bpa.13317
Publication dates
Published online11 Nov 2024
ProjectEpilepsy and Neurodegeneration: investigation into the disease mechanisms and early detection
FunderWellcome Trust

Related outputs

The prevalence of chronic traumatic encephalopathy in a historical epilepsy post‐mortem collection
Ryniejska, Maritchka, El‐Hachami, Hanaa, Mrzyglod, Alicja, Liu, Joan and Thom, M. 2024. The prevalence of chronic traumatic encephalopathy in a historical epilepsy post‐mortem collection. Brain Pathology. Advanced online publication. https://doi.org/10.1111/bpa.13317

Microangiopathy in temporal lobe epilepsy with diffusion MRI alterations and cognitive decline
Joan Y.W. Liu, Lawrence Binding, Isha Puntambekar, Smriti Patodia, Yau Lim, Alicja Mrzyglod, Fenglai Xiao, Shengning Pan, Remika Mito, Jane deTisi, John S Duncan, Sallie Baxendale, Matthias Koepp and Maria Thom 2024. Microangiopathy in temporal lobe epilepsy with diffusion MRI alterations and cognitive decline. Acta Neuropathologica Communications. 148 49. https://doi.org/10.1007/s00401-024-02809-8

Serotonin transporter in the temporal lobe, hippocampus and amygdala in SUDEP
Patodia, S., Somani, A., Liu, J.Y.W., Cattaneo, A., Paradisco, B., Garcia, M., Othman, M., Diehl, B., Foong, J. and Thom, M. 2022. Serotonin transporter in the temporal lobe, hippocampus and amygdala in SUDEP. Brain Pathology. 32 (5) e13074. https://doi.org/10.1111/bpa.13074

Safety of intracranial electroencephalography during functional electromagnetic resonance imaging in humans at 1.5 tesla using a head transmit RF coil: Histopathological and heat-shock immunohistochemistry observations.
Liu, Joan Y W, Hawsawi, Hassan B, Sharma, Niraj, Carmichael, David W, Diehl, Beate, Thom, Maria and Lemieux, Louis 2022. Safety of intracranial electroencephalography during functional electromagnetic resonance imaging in humans at 1.5 tesla using a head transmit RF coil: Histopathological and heat-shock immunohistochemistry observations. NeuroImage. 254 119129. https://doi.org/10.1016/j.neuroimage.2022.119129

Glial regenerative cell types in the superficial cortex in cortical dysplasia subtypes
Liu, J., Reeves, C., van der Pijl, R. and Thom, M. 2021. Glial regenerative cell types in the superficial cortex in cortical dysplasia subtypes. Epilepsy Research. 169 106529. https://doi.org/10.1016/j.eplepsyres.2020.106529

Granule Cell Dispersion in Human Temporal Lobe Epilepsy: Proteomics investigation of neurodevelopmental migratory pathways
Liu, J., Dzurova, N., Al-Kaaby, B., Millks, K., Sisodiya, S.M. and Thom, M. 2020. Granule Cell Dispersion in Human Temporal Lobe Epilepsy: Proteomics investigation of neurodevelopmental migratory pathways. Frontiers in Cellular Neuroscience. 14 53. https://doi.org/10.3389/fncel.2020.00053

Spatiotemporal dynamics of PDGFRβ expression in pericytes and glial scar formation in penetrating brain injuries in adults
Reeves, C., Jardim, A.P., Sisodiya, S.M., Thom, M. and Liu, J. 2019. Spatiotemporal dynamics of PDGFRβ expression in pericytes and glial scar formation in penetrating brain injuries in adults. Neuropathology and Applied Neurobiology. 45 (6), pp. 609-627 NAN-2018-0107.R1. https://doi.org/10.1111/nan.12539

Multinodular and vacuolating neuronal tumors in epilepsy: dysplasia or neoplasia?
Thom, M., Liu, J., Bongaarts, A., Reinten, R., Paradiso, B., Jäger, H., Reeves, C., Somani, A., An, S., Marsdon, D., McEvoy, A., Miserocchi, A., Thorne, L., Newman, F., Bucur, S., Honavar, M., Jacques, T. and Aronica, E. 2018. Multinodular and vacuolating neuronal tumors in epilepsy: dysplasia or neoplasia? Brain Pathology. 28 (2), pp. 155-171. https://doi.org/10.1111/bpa.12555

Characterising subtypes of hippocampal sclerosis and reorganization: correlation with pre and postoperative memory deficit
Prada Jardim, A., Liu, J., Baber, J., Michalak, Z., Reeves, C., Ellis, M., Novy, J., de Tisi, J., McEvoy, A., Miserocchi, A., Targas Yacubian, E., Sisodiya, S., Thompson, P. and Thom, M. 2018. Characterising subtypes of hippocampal sclerosis and reorganization: correlation with pre and postoperative memory deficit. Brain Pathology. 28 (2), pp. 143-154. https://doi.org/10.1111/BPA.12514

The ventrolateral medulla and medullary raphe in sudden unexpected death in epilepsy
Patodia, S., Somani, A., O’Hare, M., Venkateswaran, R., Liu, J., Michalak, Z., Ellis, M., Scheffer, I., Diehl, B., Sisodiya, S. and Thom, M. 2018. The ventrolateral medulla and medullary raphe in sudden unexpected death in epilepsy. Brain. 141 (6), pp. 1719-1733. https://doi.org/10.1093/brain/awy078

Doublecortin-expressing cell types in temporal lobe epilepsy
Liu, J.Y.W., Matarin, M., Reeves, C., McEvoy, A.W., Miserocchi, A., Thompson, P., Sisodiya, S.M. and Thom, M. 2018. Doublecortin-expressing cell types in temporal lobe epilepsy. Acta Neuropathologica Communications. 6, p. 60 60. https://doi.org/10.1186/s40478-018-0566-5

Nestin-expressing cell types in the temporal lobe and hippocampus: Morphology, differentiation, and proliferative capacity
Liu, J., Reeves, C., Thomas, J., McEvoy, A., Miserocchi, A., Thompson, P., Sisodiya, S. and Thom, M. 2018. Nestin-expressing cell types in the temporal lobe and hippocampus: Morphology, differentiation, and proliferative capacity. GLIA. 66 (1), pp. 62-77 23211. https://doi.org/10.1002/glia.23211

Pathology-MRI correlations in diffuse low-grade epilepsy associated tumors
Al-Hajri, A., Al-Mughairi, S., Somani, A., An, S., Liu, J.Y.W., Miserocchi, A., McEvoy, A.W., Yousry, T., Hoskote, C. and Thom, M. 2017. Pathology-MRI correlations in diffuse low-grade epilepsy associated tumors. Journal of Neuropathology and Experimental Neurology. 76 (12), pp. 1023-1033. https://doi.org/10.1093/jnen/nlx090

PAX6, brain structure and function in human adults: Advanced MRI in aniridia
Yogarajah, M., Matarin, M., Vollmar, C., Thompson, P.J., Duncan, J.S., Symms, M., Moore, A.T., Liu, J.Y.W., Thom, M., van Heyningen, V. and Sisodiya, S.M. 2016. PAX6, brain structure and function in human adults: Advanced MRI in aniridia. Annals of Clinical and Translational Neurology. 3 (5), pp. 314-330. https://doi.org/10.1002/acn3.297

Combined Ex Vivo 9.4T MRI and Quantitative Histopathological Study in Normal and Pathological Neocortical Resections in Focal Epilepsy
Reeves, C., Tachrount, M., Thomas, D., Michalak, Z., Liu, J.Y.W., Ellis, M., Diehl, B., Miserocchi, A., McEvoy, A.W., Eriksson, S., Yousry, T. and Thom, M. 2016. Combined Ex Vivo 9.4T MRI and Quantitative Histopathological Study in Normal and Pathological Neocortical Resections in Focal Epilepsy. Brain Pathology. 26 (3), pp. 319-333. https://doi.org/10.1111/bpa.12298

Hyperphosphorylated tau in patients with refractory epilepsy correlates with cognitive decline: a study of temporal lobe resections
Tai, X., Koepp, M., Duncan, J., Fox, N., Thompson, P., Baxendale, S., Liu, J., Reeves, C., Michalak, Z. and Thom, M. 2016. Hyperphosphorylated tau in patients with refractory epilepsy correlates with cognitive decline: a study of temporal lobe resections. Brain. 139 (9), pp. 2441-55. https://doi.org/10.1093/brain/aww187

Early lipofuscin accumulation in Frontal Lobe Epilepsy
Liu, J., Reeves, C., Diehl, B., Coppola, A., Al-Hajri, A., Hoskote, C., Mughairy, S., Tachrount, M., Groves, M., Michalak, Z., Mills, K., McEvoy, A., Miserocchi, A., Sisodiya, S. and Thom, M. 2016. Early lipofuscin accumulation in Frontal Lobe Epilepsy. Annals of Neurology. 80, pp. 882-895. https://doi.org/10.1002/ana.24803

A cautionary note in the interpretation of human papillomavirus E6 immunohistochemistry in focal cortical dysplasia
Thom, M., Liu, J., Reeves, C., Stopps, V., Sisodiya, S.M. and Liu, J.Y.W. 2015. A cautionary note in the interpretation of human papillomavirus E6 immunohistochemistry in focal cortical dysplasia. Annals of Neurology. 77 (2), pp. 352-353. https://doi.org/10.1002/ana.24330

A comparative study of the dentate gyrus in hippocampal sclerosis in epilepsy and dementia
Bandopadhyay, R., Liu, J.Y.W., Sisodiya, S.M. and Thom, M. 2014. A comparative study of the dentate gyrus in hippocampal sclerosis in epilepsy and dementia. Neuropathology and Applied Neurobiology. 40 (2), pp. 177-190. https://doi.org/10.1111/nan.12087

High-throughput, automated quantification of white matter neurons in mild malformation of cortical development in epilepsy
Liu, J.Y.W., Ellis, M., Brooke-Ball, H., de Tisi, J., Eriksson, S.H., Brandner, S., Sisodiya, S.M. and Thom, M. 2014. High-throughput, automated quantification of white matter neurons in mild malformation of cortical development in epilepsy. Acta Neuropathologica Communications. 2 72. https://doi.org/10.1186/2051-5960-2-72

Evidence for mTOR pathway activation in a spectrum of epilepsy-associated pathologies
Liu, J.Y.W., Reeves, C., Michalak, Z., Coppola, A., Diehl, B., Sisodiya, S.M. and Thom, M. 2014. Evidence for mTOR pathway activation in a spectrum of epilepsy-associated pathologies. Acta Neuropathologica Communications. 2 71. https://doi.org/10.1186/2051-5960-2-71

In vivo P-glycoprotein function before and after epilepsy surgery
Bauer, M., Karch, R., Zeitlinger, M., Liu, J.Y.W., Koepp, M.J., Asselin, M.-C., Sisodiya, S.M., Hainfellner, J.A., Wadsak, W., Mitterhauser, M., Müller, M., Pataraia, E. and Langer, O. 2014. In vivo P-glycoprotein function before and after epilepsy surgery. Neurology. 83 (15). https://doi.org/10.1212/wnl.0000000000000858

Interictal psychosis following temporal lobe surgery: dentate gyrus pathology
Thom, M., Kensche, M., Maynard, J., Liu, J.Y.W., Reeves, C., Goc, J., Marsdon, D., Fluegel, D. and Foong, J. 2014. Interictal psychosis following temporal lobe surgery: dentate gyrus pathology. Psychological Medicine. 44 (14), pp. 3037-3049. https://doi.org/10.1017/s0033291714000452

A spatiotemporal study of gliosis in relation to depth electrode tracks in drug-resistant epilepsy
Goc, J., Liu, J.Y.W., Sisodiya, S.M. and Thom, M. 2014. A spatiotemporal study of gliosis in relation to depth electrode tracks in drug-resistant epilepsy. European Journal of Neuroscience. 39 (12), pp. 2151-2162. https://doi.org/10.1111/ejn.12548

A quantitative study of white matter hypomyelination and oligodendroglial maturation in focal cortical dysplasia type II
Shepherd, C., Liu, J., Goc, J., Martinian, L., Jacques, T.S., Sisodiya, S.M., Thom, M. and Liu, J.Y.W. 2013. A quantitative study of white matter hypomyelination and oligodendroglial maturation in focal cortical dysplasia type II. Epilepsia. 54 (5), pp. 898-908. https://doi.org/10.1111/epi.12143

P-glycoprotein expression and function in patients with temporal lobe epilepsy: A case-control study
Feldmann, M., Asselin, M.-C., Wang, S., McMahon, A., Anton-Rodriguez, J., Walker, M., Symms, M., Brown, G., Hinz, R., Matthews, J., Bauer, M., Langer, O., Thom, M., Jones, T., Vollmar, C., Duncan, J.S., Sisodiya, S.M., Koepp, M.J. and Liu, J.Y.W. 2013. P-glycoprotein expression and function in patients with temporal lobe epilepsy: A case-control study. The Lancet Neurology. 12 (8), pp. 777-785. https://doi.org/10.1016/s1474-4422(13)70109-1

Neuropathology of 16p13.11 deletion in epilepsy
Liu, J.Y.W., Kasperavičiute, D., Martinian, L., Thom, M. and Sisodiya, S.M. 2012. Neuropathology of 16p13.11 deletion in epilepsy. PLoS ONE. 7 (4). https://doi.org/10.1371/journal.pone.0034813

Neuropathology of the blood-brain barrier and pharmaco-resistance in human epilepsy
Liu, J.Y.W., Thom, M., Catarino, C.B., Martinian, L., Figarella-Branger, D., Bartolomei, F., Koepp, M. and Sisodiya, S.M. 2012. Neuropathology of the blood-brain barrier and pharmaco-resistance in human epilepsy. Brain. 135 (10), p. 3115–3133. https://doi.org/10.1093/brain/aws147

Investigation of hypoxia-inducible factor-1α in hippocampal sclerosis: A postmortem study
Feast, A., Martinian, L., Liu, J.Y.W., Catarino, C.B., Thom, M. and Sisodiya, S.M. 2012. Investigation of hypoxia-inducible factor-1α in hippocampal sclerosis: A postmortem study. Epilepsia. 53 (8), pp. 1349-1359. https://doi.org/10.1111/j.1528-1167.2012.03591.x

Variability of sclerosis along the longitudinal hippocampal axis in epilepsy: A post mortem study
Thom, M., Liagkouras, I., Martinian, L., Catarino, C.B., Sisodiya, S.M. and Liu, J.Y.W. 2012. Variability of sclerosis along the longitudinal hippocampal axis in epilepsy: A post mortem study. Epilepsy Research. 102 (1-2), pp. 45-59. https://doi.org/10.1016/j.eplepsyres.2012.04.015

Neurofibrillary tangle pathology and Braak staging in chronic epilepsy in relation to traumatic brain injury and hippocampal sclerosis: A post-mortem study
Thom, M., Liu, J.Y.W., Thompson, P., Phadke, R., Narkiewicz, M., Martinian, L., Marsdon, D., Koepp, M., Caboclo, L., Catarino, C.B. and Sisodiya, S.M. 2011. Neurofibrillary tangle pathology and Braak staging in chronic epilepsy in relation to traumatic brain injury and hippocampal sclerosis: A post-mortem study. Brain. 134 (10), pp. 2969-2981. https://doi.org/10.1093/brain/awr209

Dravet syndrome as epileptic encephalopathy: Evidence from long-term course and neuropathology
Catarino, C.B., Liu, J.Y.W., Liagkouras, I., Gibbons, V.S., Labrum, R.W., Ellis, R., Woodward, C., Davis, M.B., Smith, S.J., Cross, J.H., Appleton, R.E., Yendle, S.C., McMahon, J.M., Bellows, S.T., Jacques, T.S., Zuberi, S.M., Koepp, M.J., Martinian, L., Scheffer, I.E., Thom, M. and Sisodiya, S.M. 2011. Dravet syndrome as epileptic encephalopathy: Evidence from long-term course and neuropathology. Brain. 134 (10), pp. 2982-3010. https://doi.org/10.1093/brain/awr129

Immunolabeling recovery in archival, post-mortem, human brain tissue using modified antigen retrieval and the catalyzed signal amplification system
Liu, J.Y.W., Martinian, L., Thom, M. and Sisodiya, S.M. 2010. Immunolabeling recovery in archival, post-mortem, human brain tissue using modified antigen retrieval and the catalyzed signal amplification system. Journal of Neuroscience Methods. 190 (1), pp. 49-56. https://doi.org/10.1016/j.jneumeth.2010.04.020

Permalink - https://westminsterresearch.westminster.ac.uk/item/wx37y/the-prevalence-of-chronic-traumatic-encephalopathy-in-a-historical-epilepsy-post-mortem-collection


Share this

Usage statistics

29 total views
3 total downloads
These values cover views and downloads from WestminsterResearch and are for the period from September 2nd 2018, when this repository was created.