Validating atlas-based lesion disconnectomics in multiple sclerosis: A retrospective multi-centric study
[Display omitted] •Structural disconnectomes can be modelled without diffusion using tractography atlases.•Atlas-based and DTI-derived disconnectome topological metrics correlate strongly.•MS patient disconnectomes relate to clinical scores. The translational potential of MR-based connectivity model...
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Published in | NeuroImage clinical Vol. 32; p. 102817 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Netherlands
Elsevier Inc
01.01.2021
Elsevier |
Subjects | |
Online Access | Get full text |
ISSN | 2213-1582 2213-1582 |
DOI | 10.1016/j.nicl.2021.102817 |
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Abstract | [Display omitted]
•Structural disconnectomes can be modelled without diffusion using tractography atlases.•Atlas-based and DTI-derived disconnectome topological metrics correlate strongly.•MS patient disconnectomes relate to clinical scores.
The translational potential of MR-based connectivity modelling is limited by the need for advanced diffusion imaging, which is not part of clinical protocols for many diseases. In addition, where diffusion data is available, brain connectivity analyses rely on tractography algorithms which imply two major limitations. First, tracking algorithms are known to be sensitive to the presence of white matter lesions and therefore leading to interpretation pitfalls and poor inter-subject comparability in clinical applications such as multiple sclerosis. Second, tractography quality is highly dependent on the acquisition parameters of diffusion sequences, leading to a trade-off between acquisition time and tractography precision.
Here, we propose an atlas-based approach to study the interplay between structural disconnectivity and lesions without requiring individual diffusion imaging. In a multi-centric setting involving three distinct multiple sclerosis datasets (containing both 1.5 T and 3 T data), we compare our atlas-based structural disconnectome computation pipeline to disconnectomes extracted from individual tractography and explore its clinical utility for reducing the gap between radiological findings and clinical symptoms in multiple sclerosis. Results using topological graph properties showed that overall, our atlas-based disconnectomes were suitable approximations of individual disconnectomes from diffusion imaging. Small-worldness was found to decrease for larger total lesion volumes thereby suggesting a loss of efficiency in brain connectivity of MS patients. Finally, the global efficiency of the created brain graph, combined with total lesion volume, allowed to stratify patients into subgroups with different clinical scores in all three cohorts. |
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AbstractList | [Display omitted]
•Structural disconnectomes can be modelled without diffusion using tractography atlases.•Atlas-based and DTI-derived disconnectome topological metrics correlate strongly.•MS patient disconnectomes relate to clinical scores.
The translational potential of MR-based connectivity modelling is limited by the need for advanced diffusion imaging, which is not part of clinical protocols for many diseases. In addition, where diffusion data is available, brain connectivity analyses rely on tractography algorithms which imply two major limitations. First, tracking algorithms are known to be sensitive to the presence of white matter lesions and therefore leading to interpretation pitfalls and poor inter-subject comparability in clinical applications such as multiple sclerosis. Second, tractography quality is highly dependent on the acquisition parameters of diffusion sequences, leading to a trade-off between acquisition time and tractography precision.
Here, we propose an atlas-based approach to study the interplay between structural disconnectivity and lesions without requiring individual diffusion imaging. In a multi-centric setting involving three distinct multiple sclerosis datasets (containing both 1.5 T and 3 T data), we compare our atlas-based structural disconnectome computation pipeline to disconnectomes extracted from individual tractography and explore its clinical utility for reducing the gap between radiological findings and clinical symptoms in multiple sclerosis. Results using topological graph properties showed that overall, our atlas-based disconnectomes were suitable approximations of individual disconnectomes from diffusion imaging. Small-worldness was found to decrease for larger total lesion volumes thereby suggesting a loss of efficiency in brain connectivity of MS patients. Finally, the global efficiency of the created brain graph, combined with total lesion volume, allowed to stratify patients into subgroups with different clinical scores in all three cohorts. The translational potential of MR-based connectivity modelling is limited by the need for advanced diffusion imaging, which is not part of clinical protocols for many diseases. In addition, where diffusion data is available, brain connectivity analyses rely on tractography algorithms which imply two major limitations. First, tracking algorithms are known to be sensitive to the presence of white matter lesions and therefore leading to interpretation pitfalls and poor inter-subject comparability in clinical applications such as multiple sclerosis. Second, tractography quality is highly dependent on the acquisition parameters of diffusion sequences, leading to a trade-off between acquisition time and tractography precision. Here, we propose an atlas-based approach to study the interplay between structural disconnectivity and lesions without requiring individual diffusion imaging. In a multi-centric setting involving three distinct multiple sclerosis datasets (containing both 1.5 T and 3 T data), we compare our atlas-based structural disconnectome computation pipeline to disconnectomes extracted from individual tractography and explore its clinical utility for reducing the gap between radiological findings and clinical symptoms in multiple sclerosis. Results using topological graph properties showed that overall, our atlas-based disconnectomes were suitable approximations of individual disconnectomes from diffusion imaging. Small-worldness was found to decrease for larger total lesion volumes thereby suggesting a loss of efficiency in brain connectivity of MS patients. Finally, the global efficiency of the created brain graph, combined with total lesion volume, allowed to stratify patients into subgroups with different clinical scores in all three cohorts. The translational potential of MR-based connectivity modelling is limited by the need for advanced diffusion imaging, which is not part of clinical protocols for many diseases. In addition, where diffusion data is available, brain connectivity analyses rely on tractography algorithms which imply two major limitations. First, tracking algorithms are known to be sensitive to the presence of white matter lesions and therefore leading to interpretation pitfalls and poor inter-subject comparability in clinical applications such as multiple sclerosis. Second, tractography quality is highly dependent on the acquisition parameters of diffusion sequences, leading to a trade-off between acquisition time and tractography precision. Here, we propose an atlas-based approach to study the interplay between structural disconnectivity and lesions without requiring individual diffusion imaging. In a multi-centric setting involving three distinct multiple sclerosis datasets (containing both 1.5 T and 3 T data), we compare our atlas-based structural disconnectome computation pipeline to disconnectomes extracted from individual tractography and explore its clinical utility for reducing the gap between radiological findings and clinical symptoms in multiple sclerosis. Results using topological graph properties showed that overall, our atlas-based disconnectomes were suitable approximations of individual disconnectomes from diffusion imaging. Small-worldness was found to decrease for larger total lesion volumes thereby suggesting a loss of efficiency in brain connectivity of MS patients. Finally, the global efficiency of the created brain graph, combined with total lesion volume, allowed to stratify patients into subgroups with different clinical scores in all three cohorts.The translational potential of MR-based connectivity modelling is limited by the need for advanced diffusion imaging, which is not part of clinical protocols for many diseases. In addition, where diffusion data is available, brain connectivity analyses rely on tractography algorithms which imply two major limitations. First, tracking algorithms are known to be sensitive to the presence of white matter lesions and therefore leading to interpretation pitfalls and poor inter-subject comparability in clinical applications such as multiple sclerosis. Second, tractography quality is highly dependent on the acquisition parameters of diffusion sequences, leading to a trade-off between acquisition time and tractography precision. Here, we propose an atlas-based approach to study the interplay between structural disconnectivity and lesions without requiring individual diffusion imaging. In a multi-centric setting involving three distinct multiple sclerosis datasets (containing both 1.5 T and 3 T data), we compare our atlas-based structural disconnectome computation pipeline to disconnectomes extracted from individual tractography and explore its clinical utility for reducing the gap between radiological findings and clinical symptoms in multiple sclerosis. Results using topological graph properties showed that overall, our atlas-based disconnectomes were suitable approximations of individual disconnectomes from diffusion imaging. Small-worldness was found to decrease for larger total lesion volumes thereby suggesting a loss of efficiency in brain connectivity of MS patients. Finally, the global efficiency of the created brain graph, combined with total lesion volume, allowed to stratify patients into subgroups with different clinical scores in all three cohorts. • Structural disconnectomes can be modelled without diffusion using tractography atlases. • Atlas-based and DTI-derived disconnectome topological metrics correlate strongly. • MS patient disconnectomes relate to clinical scores. The translational potential of MR-based connectivity modelling is limited by the need for advanced diffusion imaging, which is not part of clinical protocols for many diseases. In addition, where diffusion data is available, brain connectivity analyses rely on tractography algorithms which imply two major limitations. First, tracking algorithms are known to be sensitive to the presence of white matter lesions and therefore leading to interpretation pitfalls and poor inter-subject comparability in clinical applications such as multiple sclerosis. Second, tractography quality is highly dependent on the acquisition parameters of diffusion sequences, leading to a trade-off between acquisition time and tractography precision. Here, we propose an atlas-based approach to study the interplay between structural disconnectivity and lesions without requiring individual diffusion imaging. In a multi-centric setting involving three distinct multiple sclerosis datasets (containing both 1.5 T and 3 T data), we compare our atlas-based structural disconnectome computation pipeline to disconnectomes extracted from individual tractography and explore its clinical utility for reducing the gap between radiological findings and clinical symptoms in multiple sclerosis. Results using topological graph properties showed that overall, our atlas-based disconnectomes were suitable approximations of individual disconnectomes from diffusion imaging. Small-worldness was found to decrease for larger total lesion volumes thereby suggesting a loss of efficiency in brain connectivity of MS patients. Finally, the global efficiency of the created brain graph, combined with total lesion volume, allowed to stratify patients into subgroups with different clinical scores in all three cohorts. Graphical abstract |
ArticleNumber | 102817 |
Author | Mahdi, Mazen Fouad A-Wali Andelova, Michaela Fartaria, Mário João Vaneckova, Manuela Kober, Tobias Meuli, Reto Maréchal, Bénédicte Horakova, Dana Uher, Tomas Krasensky, Jan Ravano, Veronica Richiardi, Jonas |
Author_xml | – sequence: 1 givenname: Veronica surname: Ravano fullname: Ravano, Veronica email: veronica.ravano@epfl.ch organization: Advanced Clinical Imaging Technology, Siemens Healthcare AG, Lausanne, Switzerland – sequence: 2 givenname: Michaela surname: Andelova fullname: Andelova, Michaela organization: Department of Neurology and Center of Clinical Neuroscience, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic – sequence: 3 givenname: Mário João surname: Fartaria fullname: Fartaria, Mário João organization: Advanced Clinical Imaging Technology, Siemens Healthcare AG, Lausanne, Switzerland – sequence: 4 givenname: Mazen Fouad A-Wali surname: Mahdi fullname: Mahdi, Mazen Fouad A-Wali organization: Advanced Clinical Imaging Technology, Siemens Healthcare AG, Lausanne, Switzerland – sequence: 5 givenname: Bénédicte surname: Maréchal fullname: Maréchal, Bénédicte organization: Advanced Clinical Imaging Technology, Siemens Healthcare AG, Lausanne, Switzerland – sequence: 6 givenname: Reto surname: Meuli fullname: Meuli, Reto organization: Department of Radiology, Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland – sequence: 7 givenname: Tomas surname: Uher fullname: Uher, Tomas organization: Department of Neurology and Center of Clinical Neuroscience, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic – sequence: 8 givenname: Jan surname: Krasensky fullname: Krasensky, Jan organization: MR unit, Department of Radiology, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic – sequence: 9 givenname: Manuela surname: Vaneckova fullname: Vaneckova, Manuela organization: MR unit, Department of Radiology, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic – sequence: 10 givenname: Dana surname: Horakova fullname: Horakova, Dana organization: Department of Neurology and Center of Clinical Neuroscience, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic – sequence: 11 givenname: Tobias surname: Kober fullname: Kober, Tobias organization: Advanced Clinical Imaging Technology, Siemens Healthcare AG, Lausanne, Switzerland – sequence: 12 givenname: Jonas surname: Richiardi fullname: Richiardi, Jonas organization: Department of Radiology, Lausanne University Hospital and University of Lausanne, Lausanne, Switzerland |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34500427$$D View this record in MEDLINE/PubMed |
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Keywords | Disconnectome Diffusion imaging Topology Network neuroscience Structural connectivity Brain graphs |
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•Structural disconnectomes can be modelled without diffusion using tractography atlases.•Atlas-based and DTI-derived disconnectome... Graphical abstract The translational potential of MR-based connectivity modelling is limited by the need for advanced diffusion imaging, which is not part of clinical protocols... • Structural disconnectomes can be modelled without diffusion using tractography atlases. • Atlas-based and DTI-derived disconnectome topological metrics... |
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SubjectTerms | Algorithms Brain - diagnostic imaging Brain graphs Diffusion imaging Diffusion Tensor Imaging Disconnectome Humans Multiple Sclerosis - diagnostic imaging Network neuroscience Radiology Regular Retrospective Studies Structural connectivity Topology |
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Title | Validating atlas-based lesion disconnectomics in multiple sclerosis: A retrospective multi-centric study |
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