A data-driven model of brain volume changes in progressive supranuclear palsy
Abstract The most common clinical phenotype of progressive supranuclear palsy is Richardson syndrome, characterized by levodopa unresponsive symmetric parkinsonism, with a vertical supranuclear gaze palsy, early falls and cognitive impairment. There is currently no detailed understanding of the full...
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| Published in | Brain communications Vol. 4; no. 3; p. fcac098 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Oxford University Press
2022
|
| Subjects | |
| Online Access | Get full text |
| ISSN | 2632-1297 2632-1297 |
| DOI | 10.1093/braincomms/fcac098 |
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| Abstract | Abstract
The most common clinical phenotype of progressive supranuclear palsy is Richardson syndrome, characterized by levodopa unresponsive symmetric parkinsonism, with a vertical supranuclear gaze palsy, early falls and cognitive impairment. There is currently no detailed understanding of the full sequence of disease pathophysiology in progressive supranuclear palsy. Determining the sequence of brain atrophy in progressive supranuclear palsy could provide important insights into the mechanisms of disease progression, as well as guide patient stratification and monitoring for clinical trials. We used a probabilistic event-based model applied to cross-sectional structural MRI scans in a large international cohort, to determine the sequence of brain atrophy in clinically diagnosed progressive supranuclear palsy Richardson syndrome. A total of 341 people with Richardson syndrome (of whom 255 had 12-month follow-up imaging) and 260 controls were included in the study. We used a combination of 12-month follow-up MRI scans, and a validated clinical rating score (progressive supranuclear palsy rating scale) to demonstrate the longitudinal consistency and utility of the event-based model’s staging system. The event-based model estimated that the earliest atrophy occurs in the brainstem and subcortical regions followed by progression caudally into the superior cerebellar peduncle and deep cerebellar nuclei, and rostrally to the cortex. The sequence of cortical atrophy progresses in an anterior to posterior direction, beginning in the insula and then the frontal lobe before spreading to the temporal, parietal and finally the occipital lobe. This in vivo ordering accords with the post-mortem neuropathological staging of progressive supranuclear palsy and was robust under cross-validation. Using longitudinal information from 12-month follow-up scans, we demonstrate that subjects consistently move to later stages over this time interval, supporting the validity of the model. In addition, both clinical severity (progressive supranuclear palsy rating scale) and disease duration were significantly correlated with the predicted subject event-based model stage (P < 0.01). Our results provide new insights into the sequence of atrophy progression in progressive supranuclear palsy and offer potential utility to stratify people with this disease on entry into clinical trials based on disease stage, as well as track disease progression.
Using event-based modelling, Scotton et al. report the probabilistic sequence of brain atrophy progression in progressive supranuclear palsy. The resulting data-driven model, which is correlated with both clinical severity and disease duration, allows individual patient staging at baseline MRI scan with potential utility for clinical trial enrichment.
See Günter Höglinger (https://doi.org/10.1093/braincomms/fcac113) for a scientific commentary on this article.
Graphical Abstract
Graphical Abstract |
|---|---|
| AbstractList | The most common clinical phenotype of progressive supranuclear palsy is Richardson
syndrome, characterized by levodopa unresponsive symmetric parkinsonism, with a vertical
supranuclear gaze palsy, early falls and cognitive impairment. There is currently no
detailed understanding of the full sequence of disease pathophysiology in progressive
supranuclear palsy. Determining the sequence of brain atrophy in progressive supranuclear
palsy could provide important insights into the mechanisms of disease progression, as well
as guide patient stratification and monitoring for clinical trials. We used a
probabilistic event-based model applied to cross-sectional structural MRI scans in a large
international cohort, to determine the sequence of brain atrophy in clinically diagnosed
progressive supranuclear palsy Richardson syndrome. A total of 341 people with Richardson
syndrome (of whom 255 had 12-month follow-up imaging) and 260 controls were included in
the study. We used a combination of 12-month follow-up MRI scans, and a validated clinical
rating score (progressive supranuclear palsy rating scale) to demonstrate the longitudinal
consistency and utility of the event-based model’s staging system. The event-based model
estimated that the earliest atrophy occurs in the brainstem and subcortical regions
followed by progression caudally into the superior cerebellar peduncle and deep cerebellar
nuclei, and rostrally to the cortex. The sequence of cortical atrophy progresses in an
anterior to posterior direction, beginning in the insula and then the frontal lobe before
spreading to the temporal, parietal and finally the occipital lobe. This
in
vivo
ordering accords with the post-mortem neuropathological staging of
progressive supranuclear palsy and was robust under cross-validation. Using longitudinal
information from 12-month follow-up scans, we demonstrate that subjects consistently move
to later stages over this time interval, supporting the validity of the model. In
addition, both clinical severity (progressive supranuclear palsy rating scale) and disease
duration were significantly correlated with the predicted subject event-based model stage
(
P
< 0.01). Our results provide new insights into the sequence of
atrophy progression in progressive supranuclear palsy and offer potential utility to
stratify people with this disease on entry into clinical trials based on disease stage, as
well as track disease progression.
Using event-based modelling,
Scotton et al.
report the probabilistic
sequence of brain atrophy progression in progressive supranuclear palsy. The resulting
data-driven model, which is correlated with both clinical severity and disease duration,
allows individual patient staging at baseline MRI scan with potential utility for clinical
trial enrichment.
Graphical Abstract Abstract The most common clinical phenotype of progressive supranuclear palsy is Richardson syndrome, characterized by levodopa unresponsive symmetric parkinsonism, with a vertical supranuclear gaze palsy, early falls and cognitive impairment. There is currently no detailed understanding of the full sequence of disease pathophysiology in progressive supranuclear palsy. Determining the sequence of brain atrophy in progressive supranuclear palsy could provide important insights into the mechanisms of disease progression, as well as guide patient stratification and monitoring for clinical trials. We used a probabilistic event-based model applied to cross-sectional structural MRI scans in a large international cohort, to determine the sequence of brain atrophy in clinically diagnosed progressive supranuclear palsy Richardson syndrome. A total of 341 people with Richardson syndrome (of whom 255 had 12-month follow-up imaging) and 260 controls were included in the study. We used a combination of 12-month follow-up MRI scans, and a validated clinical rating score (progressive supranuclear palsy rating scale) to demonstrate the longitudinal consistency and utility of the event-based model’s staging system. The event-based model estimated that the earliest atrophy occurs in the brainstem and subcortical regions followed by progression caudally into the superior cerebellar peduncle and deep cerebellar nuclei, and rostrally to the cortex. The sequence of cortical atrophy progresses in an anterior to posterior direction, beginning in the insula and then the frontal lobe before spreading to the temporal, parietal and finally the occipital lobe. This in vivo ordering accords with the post-mortem neuropathological staging of progressive supranuclear palsy and was robust under cross-validation. Using longitudinal information from 12-month follow-up scans, we demonstrate that subjects consistently move to later stages over this time interval, supporting the validity of the model. In addition, both clinical severity (progressive supranuclear palsy rating scale) and disease duration were significantly correlated with the predicted subject event-based model stage (P < 0.01). Our results provide new insights into the sequence of atrophy progression in progressive supranuclear palsy and offer potential utility to stratify people with this disease on entry into clinical trials based on disease stage, as well as track disease progression. Using event-based modelling, Scotton et al. report the probabilistic sequence of brain atrophy progression in progressive supranuclear palsy. The resulting data-driven model, which is correlated with both clinical severity and disease duration, allows individual patient staging at baseline MRI scan with potential utility for clinical trial enrichment. See Günter Höglinger (https://doi.org/10.1093/braincomms/fcac113) for a scientific commentary on this article. Graphical Abstract Graphical Abstract The most common clinical phenotype of progressive supranuclear palsy is Richardson syndrome, characterized by levodopa unresponsive symmetric parkinsonism, with a vertical supranuclear gaze palsy, early falls and cognitive impairment. There is currently no detailed understanding of the full sequence of disease pathophysiology in progressive supranuclear palsy. Determining the sequence of brain atrophy in progressive supranuclear palsy could provide important insights into the mechanisms of disease progression, as well as guide patient stratification and monitoring for clinical trials. We used a probabilistic event-based model applied to cross-sectional structural MRI scans in a large international cohort, to determine the sequence of brain atrophy in clinically diagnosed progressive supranuclear palsy Richardson syndrome. A total of 341 people with Richardson syndrome (of whom 255 had 12-month follow-up imaging) and 260 controls were included in the study. We used a combination of 12-month follow-up MRI scans, and a validated clinical rating score (progressive supranuclear palsy rating scale) to demonstrate the longitudinal consistency and utility of the event-based model’s staging system. The event-based model estimated that the earliest atrophy occurs in the brainstem and subcortical regions followed by progression caudally into the superior cerebellar peduncle and deep cerebellar nuclei, and rostrally to the cortex. The sequence of cortical atrophy progresses in an anterior to posterior direction, beginning in the insula and then the frontal lobe before spreading to the temporal, parietal and finally the occipital lobe. This in vivo ordering accords with the post-mortem neuropathological staging of progressive supranuclear palsy and was robust under cross-validation. Using longitudinal information from 12-month follow-up scans, we demonstrate that subjects consistently move to later stages over this time interval, supporting the validity of the model. In addition, both clinical severity (progressive supranuclear palsy rating scale) and disease duration were significantly correlated with the predicted subject event-based model stage (P < 0.01). Our results provide new insights into the sequence of atrophy progression in progressive supranuclear palsy and offer potential utility to stratify people with this disease on entry into clinical trials based on disease stage, as well as track disease progression. The most common clinical phenotype of progressive supranuclear palsy is Richardson syndrome, characterized by levodopa unresponsive symmetric parkinsonism, with a vertical supranuclear gaze palsy, early falls and cognitive impairment. There is currently no detailed understanding of the full sequence of disease pathophysiology in progressive supranuclear palsy. Determining the sequence of brain atrophy in progressive supranuclear palsy could provide important insights into the mechanisms of disease progression, as well as guide patient stratification and monitoring for clinical trials. We used a probabilistic event-based model applied to cross-sectional structural MRI scans in a large international cohort, to determine the sequence of brain atrophy in clinically diagnosed progressive supranuclear palsy Richardson syndrome. A total of 341 people with Richardson syndrome (of whom 255 had 12-month follow-up imaging) and 260 controls were included in the study. We used a combination of 12-month follow-up MRI scans, and a validated clinical rating score (progressive supranuclear palsy rating scale) to demonstrate the longitudinal consistency and utility of the event-based model's staging system. The event-based model estimated that the earliest atrophy occurs in the brainstem and subcortical regions followed by progression caudally into the superior cerebellar peduncle and deep cerebellar nuclei, and rostrally to the cortex. The sequence of cortical atrophy progresses in an anterior to posterior direction, beginning in the insula and then the frontal lobe before spreading to the temporal, parietal and finally the occipital lobe. This ordering accords with the post-mortem neuropathological staging of progressive supranuclear palsy and was robust under cross-validation. Using longitudinal information from 12-month follow-up scans, we demonstrate that subjects consistently move to later stages over this time interval, supporting the validity of the model. In addition, both clinical severity (progressive supranuclear palsy rating scale) and disease duration were significantly correlated with the predicted subject event-based model stage ( < 0.01). Our results provide new insights into the sequence of atrophy progression in progressive supranuclear palsy and offer potential utility to stratify people with this disease on entry into clinical trials based on disease stage, as well as track disease progression. The most common clinical phenotype of progressive supranuclear palsy is Richardson syndrome, characterized by levodopa unresponsive symmetric parkinsonism, with a vertical supranuclear gaze palsy, early falls and cognitive impairment. There is currently no detailed understanding of the full sequence of disease pathophysiology in progressive supranuclear palsy. Determining the sequence of brain atrophy in progressive supranuclear palsy could provide important insights into the mechanisms of disease progression, as well as guide patient stratification and monitoring for clinical trials. We used a probabilistic event-based model applied to cross-sectional structural MRI scans in a large international cohort, to determine the sequence of brain atrophy in clinically diagnosed progressive supranuclear palsy Richardson syndrome. A total of 341 people with Richardson syndrome (of whom 255 had 12-month follow-up imaging) and 260 controls were included in the study. We used a combination of 12-month follow-up MRI scans, and a validated clinical rating score (progressive supranuclear palsy rating scale) to demonstrate the longitudinal consistency and utility of the event-based model's staging system. The event-based model estimated that the earliest atrophy occurs in the brainstem and subcortical regions followed by progression caudally into the superior cerebellar peduncle and deep cerebellar nuclei, and rostrally to the cortex. The sequence of cortical atrophy progresses in an anterior to posterior direction, beginning in the insula and then the frontal lobe before spreading to the temporal, parietal and finally the occipital lobe. This in vivo ordering accords with the post-mortem neuropathological staging of progressive supranuclear palsy and was robust under cross-validation. Using longitudinal information from 12-month follow-up scans, we demonstrate that subjects consistently move to later stages over this time interval, supporting the validity of the model. In addition, both clinical severity (progressive supranuclear palsy rating scale) and disease duration were significantly correlated with the predicted subject event-based model stage (P < 0.01). Our results provide new insights into the sequence of atrophy progression in progressive supranuclear palsy and offer potential utility to stratify people with this disease on entry into clinical trials based on disease stage, as well as track disease progression.The most common clinical phenotype of progressive supranuclear palsy is Richardson syndrome, characterized by levodopa unresponsive symmetric parkinsonism, with a vertical supranuclear gaze palsy, early falls and cognitive impairment. There is currently no detailed understanding of the full sequence of disease pathophysiology in progressive supranuclear palsy. Determining the sequence of brain atrophy in progressive supranuclear palsy could provide important insights into the mechanisms of disease progression, as well as guide patient stratification and monitoring for clinical trials. We used a probabilistic event-based model applied to cross-sectional structural MRI scans in a large international cohort, to determine the sequence of brain atrophy in clinically diagnosed progressive supranuclear palsy Richardson syndrome. A total of 341 people with Richardson syndrome (of whom 255 had 12-month follow-up imaging) and 260 controls were included in the study. We used a combination of 12-month follow-up MRI scans, and a validated clinical rating score (progressive supranuclear palsy rating scale) to demonstrate the longitudinal consistency and utility of the event-based model's staging system. The event-based model estimated that the earliest atrophy occurs in the brainstem and subcortical regions followed by progression caudally into the superior cerebellar peduncle and deep cerebellar nuclei, and rostrally to the cortex. The sequence of cortical atrophy progresses in an anterior to posterior direction, beginning in the insula and then the frontal lobe before spreading to the temporal, parietal and finally the occipital lobe. This in vivo ordering accords with the post-mortem neuropathological staging of progressive supranuclear palsy and was robust under cross-validation. Using longitudinal information from 12-month follow-up scans, we demonstrate that subjects consistently move to later stages over this time interval, supporting the validity of the model. In addition, both clinical severity (progressive supranuclear palsy rating scale) and disease duration were significantly correlated with the predicted subject event-based model stage (P < 0.01). Our results provide new insights into the sequence of atrophy progression in progressive supranuclear palsy and offer potential utility to stratify people with this disease on entry into clinical trials based on disease stage, as well as track disease progression. |
| Author | Scotton, W. J. Wijeratne, P. A. Todd, E. Rohrer, J. D. VandeVrede, L. Bocchetta, M. Alexander, D. C. Cash, D. M. Morris, H. R. Heuer, H. Rowe, J. B. Oxtoby, N. Boxer, A. |
| AuthorAffiliation | 6 Department of Clinical and Movement Neurosciences, University College London Queen Square Institute of Neurology , London, UK 1 Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London , London, UK 4 Department of Clinical Neurosciences, Cambridge University, Cambridge University Hospitals NHS Trust , Cambridge, UK 5 Medical Research Council Cognition and Brain Sciences Unit, Cambridge University , Cambridge, UK 7 Movement Disorders Centre, University College London Queen Square Institute of Neurology , London, UK 2 Centre for Medical Image Computing, Department of Computer Science, University College London , London, UK 3 Department of Neurology, Memory and Aging Center, University of California , San Francisco, CA, USA |
| AuthorAffiliation_xml | – name: 3 Department of Neurology, Memory and Aging Center, University of California , San Francisco, CA, USA – name: 5 Medical Research Council Cognition and Brain Sciences Unit, Cambridge University , Cambridge, UK – name: 4 Department of Clinical Neurosciences, Cambridge University, Cambridge University Hospitals NHS Trust , Cambridge, UK – name: 7 Movement Disorders Centre, University College London Queen Square Institute of Neurology , London, UK – name: 1 Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London , London, UK – name: 2 Centre for Medical Image Computing, Department of Computer Science, University College London , London, UK – name: 6 Department of Clinical and Movement Neurosciences, University College London Queen Square Institute of Neurology , London, UK |
| Author_xml | – sequence: 1 givenname: W. J. orcidid: 0000-0003-0607-3190 surname: Scotton fullname: Scotton, W. J. email: w.scotton@ucl.ac.uk organization: Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, UK – sequence: 2 givenname: M. orcidid: 0000-0003-1814-5024 surname: Bocchetta fullname: Bocchetta, M. organization: Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, UK – sequence: 3 givenname: E. orcidid: 0000-0003-1551-5691 surname: Todd fullname: Todd, E. organization: Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, UK – sequence: 4 givenname: D. M. orcidid: 0000-0001-7833-616X surname: Cash fullname: Cash, D. M. organization: Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, UK – sequence: 5 givenname: N. orcidid: 0000-0003-0203-3909 surname: Oxtoby fullname: Oxtoby, N. organization: Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK – sequence: 6 givenname: L. surname: VandeVrede fullname: VandeVrede, L. organization: Department of Neurology, Memory and Aging Center, University of California, San Francisco, CA, USA – sequence: 7 givenname: H. surname: Heuer fullname: Heuer, H. organization: Department of Neurology, Memory and Aging Center, University of California, San Francisco, CA, USA – sequence: 9 givenname: D. C. surname: Alexander fullname: Alexander, D. C. organization: Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK – sequence: 10 givenname: J. B. surname: Rowe fullname: Rowe, J. B. organization: Department of Clinical Neurosciences, Cambridge University, Cambridge University Hospitals NHS Trust, Cambridge, UK – sequence: 11 givenname: H. R. orcidid: 0000-0002-5473-3774 surname: Morris fullname: Morris, H. R. organization: Department of Clinical and Movement Neurosciences, University College London Queen Square Institute of Neurology, London, UK – sequence: 12 givenname: A. surname: Boxer fullname: Boxer, A. organization: Department of Neurology, Memory and Aging Center, University of California, San Francisco, CA, USA – sequence: 13 givenname: J. D. surname: Rohrer fullname: Rohrer, J. D. organization: Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, UK – sequence: 14 givenname: P. A. orcidid: 0000-0002-4885-6241 surname: Wijeratne fullname: Wijeratne, P. A. organization: Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35602649$$D View this record in MEDLINE/PubMed |
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| Keywords | event-based model disease progression machine learning biomarkers progressive supranuclear palsy |
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| PublicationDateYYYYMMDD | 2022-01-01 |
| PublicationDate_xml | – year: 2022 text: 2022-00-00 |
| PublicationDecade | 2020 |
| PublicationPlace | England |
| PublicationPlace_xml | – name: England |
| PublicationTitle | Brain communications |
| PublicationTitleAlternate | Brain Commun |
| PublicationYear | 2022 |
| Publisher | Oxford University Press |
| Publisher_xml | – name: Oxford University Press |
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The most common clinical phenotype of progressive supranuclear palsy is Richardson syndrome, characterized by levodopa unresponsive symmetric... The most common clinical phenotype of progressive supranuclear palsy is Richardson syndrome, characterized by levodopa unresponsive symmetric parkinsonism,... The most common clinical phenotype of progressive supranuclear palsy is Richardson syndrome, characterized by levodopa unresponsive symmetric parkinsonism,... |
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