Clinical relevance of paramagnetic rim lesion heterogeneity in multiple sclerosis
Abstract Objective Previous studies reveal heterogeneity in terms of paramagnetic rim lesions (PRL) associated tissue damage. We investigated the physiopathology and clinical implications of this heterogeneity. Methods In 103 MS patients (72 relapsing and 31 progressive), brain lesions were manually...
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| Format: | Article |
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Wiley
2024-12-01
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| Series: | Annals of Clinical and Translational Neurology |
| Online Access: | https://doi.org/10.1002/acn3.52220 |
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| author | Anna Stölting Colin Vanden Bulcke Serena Borrelli Céline Bugli Renaud Du Pasquier Vincent vanPesch Pietro Maggi |
| author_facet | Anna Stölting Colin Vanden Bulcke Serena Borrelli Céline Bugli Renaud Du Pasquier Vincent vanPesch Pietro Maggi |
| author_sort | Anna Stölting |
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| description | Abstract Objective Previous studies reveal heterogeneity in terms of paramagnetic rim lesions (PRL) associated tissue damage. We investigated the physiopathology and clinical implications of this heterogeneity. Methods In 103 MS patients (72 relapsing and 31 progressive), brain lesions were manually segmented on 3T 3D‐FLAIR and rim visibility was assessed with a visual confidence level score (VCLS) on 3D‐EPI phase. Using T1 relaxation time maps, lesions were categorized in long‐T1 and short‐T1. Lesion age was calculated from time of first gadolinium enhancement (N = 84 lesions). Results on clinical scores were validated in an extended cohort of 167 patients using normalized T1w‐MPRAGE lesion values. Results Rim visibility (VCLS analysis) was associated with increasing lesional T1 (P/PFDR < 0.001). Of 1680 analyzed lesions, 427 were categorized as PRL. Long‐T1 PRL were older than short‐T1 PRL (average 0.8 vs. 2.0 years, P/PFDR = 0.005/0.008), and featured larger lesional volume (P/PFDR < 0.0001) and multi‐shell diffusion‐measured axonal damage (P/PFDR < 0.0001). The total volume of long‐T1‐PRL versus PRL showed 2× predictive power for both higher MS disability (EDSS; P/PFDR = 0.003/0.005 vs. P/PFDR = 0.042/0.057) and severity (MSSS; P/PFDR = 0.0006/0.001 vs. P/PFDR = 0.004/0.007). In random forest, having ≥1 long‐T1‐PRL versus ≥4 PRL showed 2‐4× higher performance to predict a higher EDSS and MSSS. In the validation cohort, long‐T1 PRL outperformed (~2×) PRL in predicting both EDSS and MSSS. Interpretation PRL show substantial heterogeneity in terms of intralesional tissue damage. More destructive, likely older, long‐T1 PRL improve the association with MS clinical scales. This PRL heterogeneity characterization was replicated using standard T1w MRI, highlighting its potential for clinical translation. |
| format | Article |
| id | doaj-art-5fc1ef95d3ba4a4eaaeea857eab8bd60 |
| institution | Kabale University |
| issn | 2328-9503 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Wiley |
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| series | Annals of Clinical and Translational Neurology |
| spelling | doaj-art-5fc1ef95d3ba4a4eaaeea857eab8bd602024-12-17T16:12:21ZengWileyAnnals of Clinical and Translational Neurology2328-95032024-12-0111123137315110.1002/acn3.52220Clinical relevance of paramagnetic rim lesion heterogeneity in multiple sclerosisAnna Stölting0Colin Vanden Bulcke1Serena Borrelli2Céline Bugli3Renaud Du Pasquier4Vincent vanPesch5Pietro Maggi6Neuroinflammation Imaging Lab (NIL) Institute of NeuroScience, Université catholique de Louvain Brussels BelgiumNeuroinflammation Imaging Lab (NIL) Institute of NeuroScience, Université catholique de Louvain Brussels BelgiumNeuroinflammation Imaging Lab (NIL) Institute of NeuroScience, Université catholique de Louvain Brussels BelgiumPlateforme technologique de Support en Méthodologie et Calcul Statistique Université catholique de Louvain Brussels BelgiumNeurology Service, Department of Clinical Neurosciences University Hospital of Lausanne and University of Lausanne Lausanne SwitzerlandDepartment of Neurology Cliniques universitaires Saint‐Luc, Université catholique de Louvain Brussels BelgiumNeuroinflammation Imaging Lab (NIL) Institute of NeuroScience, Université catholique de Louvain Brussels BelgiumAbstract Objective Previous studies reveal heterogeneity in terms of paramagnetic rim lesions (PRL) associated tissue damage. We investigated the physiopathology and clinical implications of this heterogeneity. Methods In 103 MS patients (72 relapsing and 31 progressive), brain lesions were manually segmented on 3T 3D‐FLAIR and rim visibility was assessed with a visual confidence level score (VCLS) on 3D‐EPI phase. Using T1 relaxation time maps, lesions were categorized in long‐T1 and short‐T1. Lesion age was calculated from time of first gadolinium enhancement (N = 84 lesions). Results on clinical scores were validated in an extended cohort of 167 patients using normalized T1w‐MPRAGE lesion values. Results Rim visibility (VCLS analysis) was associated with increasing lesional T1 (P/PFDR < 0.001). Of 1680 analyzed lesions, 427 were categorized as PRL. Long‐T1 PRL were older than short‐T1 PRL (average 0.8 vs. 2.0 years, P/PFDR = 0.005/0.008), and featured larger lesional volume (P/PFDR < 0.0001) and multi‐shell diffusion‐measured axonal damage (P/PFDR < 0.0001). The total volume of long‐T1‐PRL versus PRL showed 2× predictive power for both higher MS disability (EDSS; P/PFDR = 0.003/0.005 vs. P/PFDR = 0.042/0.057) and severity (MSSS; P/PFDR = 0.0006/0.001 vs. P/PFDR = 0.004/0.007). In random forest, having ≥1 long‐T1‐PRL versus ≥4 PRL showed 2‐4× higher performance to predict a higher EDSS and MSSS. In the validation cohort, long‐T1 PRL outperformed (~2×) PRL in predicting both EDSS and MSSS. Interpretation PRL show substantial heterogeneity in terms of intralesional tissue damage. More destructive, likely older, long‐T1 PRL improve the association with MS clinical scales. This PRL heterogeneity characterization was replicated using standard T1w MRI, highlighting its potential for clinical translation.https://doi.org/10.1002/acn3.52220 |
| spellingShingle | Anna Stölting Colin Vanden Bulcke Serena Borrelli Céline Bugli Renaud Du Pasquier Vincent vanPesch Pietro Maggi Clinical relevance of paramagnetic rim lesion heterogeneity in multiple sclerosis Annals of Clinical and Translational Neurology |
| title | Clinical relevance of paramagnetic rim lesion heterogeneity in multiple sclerosis |
| title_full | Clinical relevance of paramagnetic rim lesion heterogeneity in multiple sclerosis |
| title_fullStr | Clinical relevance of paramagnetic rim lesion heterogeneity in multiple sclerosis |
| title_full_unstemmed | Clinical relevance of paramagnetic rim lesion heterogeneity in multiple sclerosis |
| title_short | Clinical relevance of paramagnetic rim lesion heterogeneity in multiple sclerosis |
| title_sort | clinical relevance of paramagnetic rim lesion heterogeneity in multiple sclerosis |
| url | https://doi.org/10.1002/acn3.52220 |
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