Quantification of Lewy body pathology by cerebrospinal fluid endpoint dilution RT-QuIC in a neuropathological autopsy cohort of clinically heterogeneous participants
(2025) In Acta Neuropathologica 149(1).- Abstract
The identification of biomarkers predicting the burden of brain alpha-synuclein (α-syn) pathology in vivo represents a research priority in Lewy body disease (LBD). Recently, some kinetic parameters of seed amplification assays (SAAs) for α-syn showed associations with measures of clinical progression. However, preanalytical and analytical factors significantly affect these parameters, reducing reproducibility. The Endpoint Dilution (ED) SAA Real-time Quaking-induced Conversion (RT-QuIC) is emerging as an alternative, more accurate tool for seed quantification. Still, the approach needs validation in large patient cohorts. We applied the ED RT-QuIC to postmortem ventricular cerebrospinal fluid (CSF) samples from 357 brain donors,... (More)
The identification of biomarkers predicting the burden of brain alpha-synuclein (α-syn) pathology in vivo represents a research priority in Lewy body disease (LBD). Recently, some kinetic parameters of seed amplification assays (SAAs) for α-syn showed associations with measures of clinical progression. However, preanalytical and analytical factors significantly affect these parameters, reducing reproducibility. The Endpoint Dilution (ED) SAA Real-time Quaking-induced Conversion (RT-QuIC) is emerging as an alternative, more accurate tool for seed quantification. Still, the approach needs validation in large patient cohorts. We applied the ED RT-QuIC to postmortem ventricular cerebrospinal fluid (CSF) samples from 357 brain donors, including 168 who showed LBD at neuropathologic examination. We estimated the seeding dose, yielding positive responses in 50% of replicate reactions (SD50), using the midSIN algorithm and correlated these values with postmortem synuclein pathology burden and clinical severity measures. LBD was staged through the Unified Staging System for Lewy Body Disorders and the Lewy pathology consensus criteria. The SD50 values (expressed in log10SD/ml) differed significantly among participants at different LBD stages (p < 0.0001), with those at a neocortical stage demonstrating higher values than those at a brainstem-predominant stage (p < 0.0001). The SD50 values were significantly associated with the LBD load evaluated through immunohistochemistry (Rho = 0.62, p < 0.0001). Participants showing higher SD50 values performed worse at the last available scores on clinical scales evaluating motor (Rho = 0.33, p < 0.0001) and olfactory functions (Rho = − 0.33, p < 0.0001). The SD50 scores accurately distinguished neocortical LBD participants from those at lower stages (area under the curve, 0.86; 95% confidence interval, 0.79–0.92). The CSF ED RT-QuIC measure of α-syn seeds correlated significantly with LBD burden and clinical severity scores. These findings validate the CSF ED RT-QuIC as a quantitative assay for misfolded brain α-syn in LBD. This novel approach may be clinically applied to identify individuals at different stages of LBD pathology in research settings.
(Less)
- author
- organization
- publishing date
- 2025-06
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- Alpha-synuclein, Autopsy, Endpoint dilution, Lewy body disease, SD50, Seed amplification assay, Staging
- in
- Acta Neuropathologica
- volume
- 149
- issue
- 1
- article number
- 67
- publisher
- Springer
- external identifiers
-
- pmid:40549179
- scopus:105008800452
- ISSN
- 0001-6322
- DOI
- 10.1007/s00401-025-02904-4
- language
- English
- LU publication?
- yes
- additional info
- Publisher Copyright: © The Author(s) 2025.
- id
- 69bdda5d-5236-4dbc-a191-4c08f1cc5407
- date added to LUP
- 2025-12-16 11:34:12
- date last changed
- 2025-12-17 03:00:19
@article{69bdda5d-5236-4dbc-a191-4c08f1cc5407,
abstract = {{<p>The identification of biomarkers predicting the burden of brain alpha-synuclein (α-syn) pathology in vivo represents a research priority in Lewy body disease (LBD). Recently, some kinetic parameters of seed amplification assays (SAAs) for α-syn showed associations with measures of clinical progression. However, preanalytical and analytical factors significantly affect these parameters, reducing reproducibility. The Endpoint Dilution (ED) SAA Real-time Quaking-induced Conversion (RT-QuIC) is emerging as an alternative, more accurate tool for seed quantification. Still, the approach needs validation in large patient cohorts. We applied the ED RT-QuIC to postmortem ventricular cerebrospinal fluid (CSF) samples from 357 brain donors, including 168 who showed LBD at neuropathologic examination. We estimated the seeding dose, yielding positive responses in 50% of replicate reactions (SD50), using the midSIN algorithm and correlated these values with postmortem synuclein pathology burden and clinical severity measures. LBD was staged through the Unified Staging System for Lewy Body Disorders and the Lewy pathology consensus criteria. The SD50 values (expressed in log<sub>10</sub>SD/ml) differed significantly among participants at different LBD stages (p < 0.0001), with those at a neocortical stage demonstrating higher values than those at a brainstem-predominant stage (p < 0.0001). The SD50 values were significantly associated with the LBD load evaluated through immunohistochemistry (Rho = 0.62, p < 0.0001). Participants showing higher SD50 values performed worse at the last available scores on clinical scales evaluating motor (Rho = 0.33, p < 0.0001) and olfactory functions (Rho = − 0.33, p < 0.0001). The SD50 scores accurately distinguished neocortical LBD participants from those at lower stages (area under the curve, 0.86; 95% confidence interval, 0.79–0.92). The CSF ED RT-QuIC measure of α-syn seeds correlated significantly with LBD burden and clinical severity scores. These findings validate the CSF ED RT-QuIC as a quantitative assay for misfolded brain α-syn in LBD. This novel approach may be clinically applied to identify individuals at different stages of LBD pathology in research settings.</p>}},
author = {{Mastrangelo, Andrea and Caldera, Serena and Mastenbroek, Sophie E. and Vittoriosi, Erica and Janelidze, Shorena and Serrano, Geidy E. and Atri, Alireza and Shill, Holly and Driver-Dunckley, Erika and Mehta, Shyamal and Adler, Charles H. and Mammana, Angela and Magliocchetti, Franco and Baiardi, Simone and Beach, Thomas G. and Hansson, Oskar and Parchi, Piero}},
issn = {{0001-6322}},
keywords = {{Alpha-synuclein; Autopsy; Endpoint dilution; Lewy body disease; SD50; Seed amplification assay; Staging}},
language = {{eng}},
number = {{1}},
publisher = {{Springer}},
series = {{Acta Neuropathologica}},
title = {{Quantification of Lewy body pathology by cerebrospinal fluid endpoint dilution RT-QuIC in a neuropathological autopsy cohort of clinically heterogeneous participants}},
url = {{http://dx.doi.org/10.1007/s00401-025-02904-4}},
doi = {{10.1007/s00401-025-02904-4}},
volume = {{149}},
year = {{2025}},
}
