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Fulminant corticobasal degeneration: a distinct variant with predominant neuronal tau aggregates

Fulminant corticobasal degeneration: a distinct variant with predominant neuronal tau aggregates
Fulminant corticobasal degeneration: a distinct variant with predominant neuronal tau aggregates
Corticobasal degeneration typically progresses gradually over 5–7 years from onset till death. Fulminant corticobasal degeneration cases with a rapidly progressive course were rarely reported (RP-CBD). This study aimed to investigate their neuropathological characteristics. Of the 124 autopsy-confirmed corticobasal degeneration cases collected from 14 centres, we identified 6 RP-CBD cases (4.8%) who died of advanced disease within 3 years of onset. These RP-CBD cases had different clinical phenotypes including rapid global cognitive decline (N = 2), corticobasal syndrome (N = 2) and Richardson’s syndrome (N = 2). We also studied four corticobasal degeneration cases with an average disease duration of 3 years or less, who died of another unrelated illness (Intermediate-CBD). Finally, we selected 12 age-matched corticobasal degeneration cases out of a cohort of 110, who had a typical gradually progressive course and reached advanced clinical stage (End-stage-CBD). Quantitative analysis showed high overall tau burden (p = 0.2) and severe nigral cell loss (p = 0.47) in both the RP-CBD and End-stage-CBD groups consistent with advanced pathological changes, while the Intermediate-CBD group (mean disease duration = 3 years) had milder changes than End-stage-CBD (p < 0.05). These findings indicated that RP-CBD cases had already developed advanced pathological changes as those observed in End-stage-CBD cases (mean disease duration = 6.7 years), but within a significantly shorter duration (2.5 years; p < 0.001). Subgroup analysis was performed to investigate the cellular patterns of tau aggregates in the anterior frontal cortex and caudate by comparing neuronal-to-astrocytic plaque ratios between six RP-CBD cases, four Intermediate-CBD and 12 age-matched End-stage-CBD. Neuronal-to-astrocytic plaque ratios of Intermediate-CBD and End-stage-CBD, but not RP-CBD, positively correlated with disease duration in both the anterior frontal cortex and caudate (p = 0.02). In contrast to the predominance of astrocytic plaques we previously reported in preclinical asymptomatic corticobasal degeneration cases, neuronal tau aggregates predominated in RP-CBD exceeding those in Intermediate-CBD (anterior frontal cortex: p < 0.001, caudate: p = 0.001) and End-stage-CBD (anterior frontal cortex: p = 0.03, caudate: p = 0.01) as demonstrated by its higher neuronal-to-astrocytic plaque ratios in both anterior frontal cortex and caudate. We did not identify any difference in age at onset, any pathogenic tau mutation or concomitant pathologies that could have contributed to the rapid progression of these RP-CBD cases. Mild TDP-43 pathology was observed in three RP-CBD cases. All RP-CBD cases were men. The MAPT H2 haplotype, known to be protective, was identified in one RP-CBD case (17%) and 8 of the matched End-stage-CBD cases (67%). We conclude that RP-CBD is a distinct aggressive variant of corticobasal degeneration with characteristic neuropathological substrates resulting in a fulminant disease process as evident both clinically and pathologically. Biological factors such as genetic modifiers likely play a pivotal role in the RP-CBD variant and should be the subject of future research.
Astrocytic plaques, Corticobasal degeneration, Neurofibrillary tangles, Progressive supranuclear palsy, Tau
0001-6322
717-734
Ling, Helen
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Gelpi, Ellen
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Davey, Karen
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Jaunmuktane, Zane
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Mok, Kin Y.
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Jabbari, Edwin
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Simone, Roberto
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R’bibo, Lea
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Brandner, Sebastian
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Ellis, Matthew J.
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Attems, Johannes
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Mann, David
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Halliday, Glenda M.
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Al-sarraj, S.
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Hedreen, J.
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Ironside, James W.
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Kovacs, Gabor G.
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Kovari, E.
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Love, S.
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Vonsattel, Jean Paul G.
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Allinson, Kieren S. J.
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Hansen, Daniela
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Bradshaw, Teisha
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Setó-salvia, Núria
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Wray, Selina
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De Silva, Rohan
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Morris, Huw R.
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Warner, Thomas T.
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Hardy, John
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Holton, Janice L.
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Revesz, Tamas
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Ling, Helen
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Gelpi, Ellen
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Davey, Karen
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Jaunmuktane, Zane
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Mok, Kin Y.
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Jabbari, Edwin
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Simone, Roberto
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R’bibo, Lea
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Brandner, Sebastian
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Ellis, Matthew J.
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Attems, Johannes
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Mann, David
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Halliday, Glenda M.
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Al-sarraj, S.
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Hedreen, J.
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Ironside, James W.
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Kovacs, Gabor G.
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Kovari, E.
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Love, S.
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Vonsattel, Jean Paul G.
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Allinson, Kieren S. J.
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Hansen, Daniela
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Bradshaw, Teisha
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Setó-salvia, Núria
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Wray, Selina
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De Silva, Rohan
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Morris, Huw R.
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Warner, Thomas T.
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Hardy, John
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Holton, Janice L.
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Revesz, Tamas
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Ling, Helen, Gelpi, Ellen, Davey, Karen, Jaunmuktane, Zane, Mok, Kin Y., Jabbari, Edwin, Simone, Roberto, R’bibo, Lea, Brandner, Sebastian, Ellis, Matthew J., Attems, Johannes, Mann, David, Halliday, Glenda M., Al-sarraj, S., Hedreen, J., Ironside, James W., Kovacs, Gabor G., Kovari, E., Love, S., Vonsattel, Jean Paul G., Allinson, Kieren S. J., Hansen, Daniela, Bradshaw, Teisha, Setó-salvia, Núria, Wray, Selina, De Silva, Rohan, Morris, Huw R., Warner, Thomas T., Hardy, John, Holton, Janice L. and Revesz, Tamas (2020) Fulminant corticobasal degeneration: a distinct variant with predominant neuronal tau aggregates. Acta Neuropathologica, 139 (4), 717-734. (doi:10.1007/s00401-019-02119-4).

Record type: Article

Abstract

Corticobasal degeneration typically progresses gradually over 5–7 years from onset till death. Fulminant corticobasal degeneration cases with a rapidly progressive course were rarely reported (RP-CBD). This study aimed to investigate their neuropathological characteristics. Of the 124 autopsy-confirmed corticobasal degeneration cases collected from 14 centres, we identified 6 RP-CBD cases (4.8%) who died of advanced disease within 3 years of onset. These RP-CBD cases had different clinical phenotypes including rapid global cognitive decline (N = 2), corticobasal syndrome (N = 2) and Richardson’s syndrome (N = 2). We also studied four corticobasal degeneration cases with an average disease duration of 3 years or less, who died of another unrelated illness (Intermediate-CBD). Finally, we selected 12 age-matched corticobasal degeneration cases out of a cohort of 110, who had a typical gradually progressive course and reached advanced clinical stage (End-stage-CBD). Quantitative analysis showed high overall tau burden (p = 0.2) and severe nigral cell loss (p = 0.47) in both the RP-CBD and End-stage-CBD groups consistent with advanced pathological changes, while the Intermediate-CBD group (mean disease duration = 3 years) had milder changes than End-stage-CBD (p < 0.05). These findings indicated that RP-CBD cases had already developed advanced pathological changes as those observed in End-stage-CBD cases (mean disease duration = 6.7 years), but within a significantly shorter duration (2.5 years; p < 0.001). Subgroup analysis was performed to investigate the cellular patterns of tau aggregates in the anterior frontal cortex and caudate by comparing neuronal-to-astrocytic plaque ratios between six RP-CBD cases, four Intermediate-CBD and 12 age-matched End-stage-CBD. Neuronal-to-astrocytic plaque ratios of Intermediate-CBD and End-stage-CBD, but not RP-CBD, positively correlated with disease duration in both the anterior frontal cortex and caudate (p = 0.02). In contrast to the predominance of astrocytic plaques we previously reported in preclinical asymptomatic corticobasal degeneration cases, neuronal tau aggregates predominated in RP-CBD exceeding those in Intermediate-CBD (anterior frontal cortex: p < 0.001, caudate: p = 0.001) and End-stage-CBD (anterior frontal cortex: p = 0.03, caudate: p = 0.01) as demonstrated by its higher neuronal-to-astrocytic plaque ratios in both anterior frontal cortex and caudate. We did not identify any difference in age at onset, any pathogenic tau mutation or concomitant pathologies that could have contributed to the rapid progression of these RP-CBD cases. Mild TDP-43 pathology was observed in three RP-CBD cases. All RP-CBD cases were men. The MAPT H2 haplotype, known to be protective, was identified in one RP-CBD case (17%) and 8 of the matched End-stage-CBD cases (67%). We conclude that RP-CBD is a distinct aggressive variant of corticobasal degeneration with characteristic neuropathological substrates resulting in a fulminant disease process as evident both clinically and pathologically. Biological factors such as genetic modifiers likely play a pivotal role in the RP-CBD variant and should be the subject of future research.

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Accepted/In Press date: 20 December 2019
e-pub ahead of print date: 16 January 2020
Published date: 1 April 2020
Additional Information: Funding Information: This project is funded by a Karin & Sten Mortstedt CBD Solutions research grant (Grant code: 512385). H.L. presented this work at the British Neuropathological Society Annual Meeting in 2018 and at the 1st International Research Symposium on PSP & CBD in 2018. This research was partly supported by the National Institute for Health Research (NIHR) Queen Square Biomedical Research Unit in Dementia based at University College London Hospitals (UCLH), University College London (UCL). The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health. Acknowledgements Funding Information: The authors thank all patients and their families for their support of this research, our UK and international collaborators for their contributions to this project. Tissue collection by the Sydney Brain Bank is supported by the University of New South Wales and Neuroscience Research Australia. We thank all the past and present fellows at the Queen Square Brain Bank for their valuable contribution to the medical records of some of these patients during life and clinical summaries after brain donation especially Alastair Noyce, Nadia Magdalinou and Atbin Djamshidian, Jonathan Bestwick for his statistic advice, colleagues at the Queen Square Brain Bank for tissue preparation (Linda Parsons, Geshanthi Hondhamuni, Kate Strand, Rob Courtney) and database search (Mina Creathorn) and UCL Institute of Neurology medical illustration for their assistance. Funding Information: H.L. K.D., K.Y.M, R.S, T.B, S.W., N.S-S, R. dS., H.R.M, J.H., T.T.W., J.L.H., T.R. receive research grant from Karin & Sten Mortstedt CBD Solutions. EG received a grant from the Fundació Marató de TV3 (Grant number: 20141610). GMH is supported by an NHMRC Senior Principal Research Fellowship. H.R.M. receives research grant from the PSP Association. E.J. is supported by a MRC Fellowship. M.J.E. receives funding from Cancer Research UK Accelerator Grant (C1 15121 A 20256). Other authors report no conflict of interest. Publisher Copyright: © 2020, The Author(s).
Keywords: Astrocytic plaques, Corticobasal degeneration, Neurofibrillary tangles, Progressive supranuclear palsy, Tau

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Local EPrints ID: 437561
URI: http://eprints.soton.ac.uk/id/eprint/437561
ISSN: 0001-6322
PURE UUID: 44e9b802-0a62-4cc3-a53b-97952fdabb99

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Date deposited: 05 Feb 2020 17:32
Last modified: 16 Mar 2024 06:25

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Contributors

Author: Helen Ling
Author: Ellen Gelpi
Author: Karen Davey
Author: Zane Jaunmuktane
Author: Kin Y. Mok
Author: Edwin Jabbari
Author: Roberto Simone
Author: Lea R’bibo
Author: Sebastian Brandner
Author: Matthew J. Ellis
Author: Johannes Attems
Author: David Mann
Author: Glenda M. Halliday
Author: S. Al-sarraj
Author: J. Hedreen
Author: James W. Ironside
Author: Gabor G. Kovacs
Author: E. Kovari
Author: S. Love
Author: Jean Paul G. Vonsattel
Author: Kieren S. J. Allinson
Author: Daniela Hansen
Author: Teisha Bradshaw
Author: Núria Setó-salvia
Author: Selina Wray
Author: Rohan De Silva
Author: Huw R. Morris
Author: Thomas T. Warner
Author: John Hardy
Author: Janice L. Holton
Author: Tamas Revesz

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