Abstract
Background
Motor capacity is crucial in amyotrophic lateral sclerosis (ALS) clinical trial design and patient care. However, few studies have explored the potential of multimodal MRI to predict motor capacity in ALS. This study aims to evaluate the predictive value of cervical spinal cord MRI parameters for motor capacity in ALS compared to clinical prognostic factors.
Methods
Spinal multimodal MRI was performed shortly after diagnosis in 41 ALS patients and 12 healthy participants as part of a prospective multicenter cohort study, the PULSE study (NCT 2013-A00969-36). Motor capacity was assessed using ALSFRS-R scores. Multiple stepwise linear regression models were constructed to predict motor capacity at 3 and 6 months from diagnosis, based on clinical variables, structural MRI measurements, including spinal cord cross-sectional area (CSA), anterior–posterior, and left-to-right cross-section diameters at vertebral levels from C1 to T4, and diffusion parameters in the lateral corticospinal tracts (LCSTs) and dorsal columns.
Results
Structural MRI measurements were significantly correlated with the ALSFRS-R score and its sub-scores. And as early as 3 months from diagnosis, structural MRI measurements fit the best multiple linear regression model to predict the total ALSFRS-R (R2 = 0.70, p value = 0.0001) and arm sub-score (R2 = 0.69, p value = 0.0002), and combined with DTI metric in the LCST and clinical factors fit the best multiple linear regression model to predict leg sub-score (R2 = 0.73, p value = 0.0002).
Conclusions
Spinal multimodal MRI could be promising as a tool to enhance prognostic accuracy and serve as a motor function proxy in ALS.
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Abbreviations
- AAE:
-
Average absolute error
- AD:
-
Axial diffusivity
- ALS:
-
Amyotrophic lateral sclerosis
- ALSFRS-R:
-
ALS functional rating scale-revised
- APD:
-
Anterior–posterior diameter
- RLD:
-
Right-left diameter
- CSA:
-
Cross-sectional area
- DC:
-
Dorsal columns
- DTI:
-
Diffusion tensor imaging
- EPI:
-
Echoplanar imaging
- FA:
-
Fractional anisotropy
- FOV:
-
Field of view
- HC:
-
Healthy control
- LCST:
-
Lateral corticospinal tracts
- LMN:
-
Lower motor neuron
- MD:
-
Mean diffusivity
- MRI:
-
Magnetic resonance imaging
- R 2 :
-
R-Square
- RASE:
-
Relative average squared error
- RD:
-
Radial diffusivity
- SCT:
-
Spinal Cord Toolbox
- SD:
-
Standard deviation
- TSE:
-
Turbo spin-echo
- UMN:
-
Upper motor neuron
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Acknowledgements
The authors would like to express their gratitude to all the participants and their families for their cooperation. The research was generously supported by the French ARSLA charity (Christine Tabuenca, Marie FranceCazalère, Sabine Turgeman, and Valérie Goutines), as well as the French clinical research networks FILSLAN and ACT4ALS-MND. The authors are also grateful to the Fédération de la Recherche Clinique du CHU de Lille for their invaluable support (Anne-Sophie Rolland, Alain Duhamel, Maeva Kheng, Julien Labreuch, Dominique Deplanque, Edouard Millois, Victor Laugeais, Maxime Caillier, Aymen Aouni, Pauline Guyon, Francine Niset, Valérie Santraine, Marie Pleuvret, Mathilde Bon and Laetitia Thibault). We also thank the neurologists who participated in the recruitment of the patients. We thank the Center for NeuroImaging Research (CENIR), the CATI platform especially Marie Chupin and Fouzia El-Mountassir, and the Center for Clinical Investigation, especially Nadia Osman and Vanessa Brochard, in the Brain Institute (Pitié-Salpêtrière Hospital, Paris, France).
Lille Neurologists: Dr Veronique Danel-Brunaud, Pr Caroline Moreau. Pneumologists: Dr Thierry Perez. Neuroradiologists: Dumont. Neuropsychologists: Pr K Dujardin. Neurophysiologists: Dr Arnaud Delval; Biologists: Patrick Gelé. Clinical Assistant: Marie Pleuvret, Valerie Santraine, Francine Niset, Julien Dumont, Victor Laugeais, Mathilde Bon. Clinical trials vigilance unit: Thavarak Ouk, Camille Potey, Celine Leclercq, Elise Gers. Paris Neurologists: Dr Francois Salachas, Dr Pierre-François Pradat, Dr Gaelle Bruneteau. Neuropsychologists: Dr Lucette Lacomblez, Julie Socha, Fanny Pineau. Neurophysiologists: Dr Timothee Lenglet. Biologists: Patricia Doucelance Stéphanie Folhinha. Clinical Assistant: Amandine Bordet, Hugo Royer, Nadia Osman, Sabah Ait Khelifa. Tours Neurologists: Dr Philippe Corcia, Dr Stephane Beltran; Pneumologists: Dr Delphine Carmier. Neuroradiologists: Dr Laurent Barantin. Biologists: Hélène Blasco. Clinical Assistant: Salah Eddine Bakkouche, Mohad Mouzouri. Saint-Etienne Neurologists: Pr Jean-Christophe Antoine, Pr Jean-Philippe Camdessanché, Dr Nathalie Dimier, Dr Anne-Laure Kaminsky. Pneumologists: Dr Isabelle Court-Fortune. Neuroradiologists: Dr Claire Boutet. Biologists: Philippe Gonzalo. Clinical Assistant: Vincent Visneux, Karine Ferraud, Georgette Berlier. Brest Neurologists: Dr Steeve Genestet. Pneumologists: Dr Christophe Gut-Gobert. Neuroradiologists: Pr Douraied Ben Salem. Neuropsychologists: Pauline Nicolas, Sabine Larvor; . Biologists: Kevin Mouly, Liana Le Roux, Kevin Postec, Camille Bezeazux, Sylvain Rosec. Clinical Assistant: Hélène Fortin-Prunier, Gaelle Novert, Elsa Menanteau, Kevin Postec, Magali Denizot. Lyon Neurologists: Dr Emilien Bernard, Dr Christophe Vial, Pr Emmanuel Broussole, Dr Juliette Svahn. Pneumologists: Dr Pierre Le Cam; Neuroradiologists: Pr Yves Berthezene, Philippe Combet. Neuropsychologists: Sophie Jacqueline. Clinical Assistant: Camille Neuillet, Adeline Mansuy. Montpellier Neurologists: Pr William Camu, Dr Juntas-Morates, Dr Pageot, Dr Esselin. Neuroradiologists: Dr Champfleur. Neuropsychologists: Roy-Bellina. Biologists: Pr Sylvain Lehmann. Clinical Assistant: Sebastien Alphandry, Laura Labar, Leandra Baudesson. Marseille Neurologists: Pr Sharam Attarian, Dr Aude-Marie Grapperon, Pr Jean Pouget, Dr Annie Verschueren, Dr Jaochim Bas. Pneumologists: Dr Armelle Finet-Monnier. Neuropsychologists: Carole Belingher. Clinical Assistant: Saran Diallo, Nacime Heddadji, Sebastien Alphandery, Leandra Baudesson; Nurse: Pascale Reginensi. Nice Neurologists: Dr Claude Desnuelle, Dr Marie-Hélene Soriani. Neuroradiologists: Dr S Chanalet, Dr Lydiane Mondot. Neurophysiologists: Dr Puma; Biologists: Pr Isabelle Pruvost. Clinical Assistant: Carole Barré. Toulouse Neurologists: Dr Pascal Cintas, Dr Marie-Christine Arne Bes, Dr Blandine Acket, Dr Jérémie Pariente, Dr Isabelle Guilbaud. Neuroradiologists: Pr Fabrice Bonneville. Biologists: Dr E Causse. Physical therapists: Thierry Lagarde. Nutritionists: Jeremy Geffroy. Clinical Assistant: Magali Centelles, Véronique Hermet-Douard. Nancy Neurologists: Dr Sophie Pittion-Vouyovitch, Dr Maud Michon. Neuropsychologists: Mylène Meyer; Biologists: Sandra Lomazzi. Clinical Assistant: Gabriella Hossu, Anne Chatelain. Limoges Neurologists: Pr Philippe Couratier, Dr Geraldine Lautrette. Pneumologists: Dr Francois Vincent, Dr Larie-Therese Antonini, Dr Florent Favard. Neuroradiologists: Dr MLArie-Paule Boncoeur-Martel. Neuropsychologists: Marianne Chouly. Nutritionists: Pr Jean-Claude Desport, Dr Pierre Jesus, Dr Phillipe Fayemendy. Clinical Assistant: Clémence Labetoulle, Julie Catteau, Olivier Villeneuve. Nurse: Selam Machat. Clermont-Ferrand Neurologists: Dr Nathalie Guy, Pr Pierre Clavelou. Pneumologists: Dr Anick Greil, Pr M Duclos. Neuroradiologists: Dr Betty Jean, Dr Carine Chassain, Camille Tsoutsos, Claudine Speziale, Aurélie Cladiere. Nutritionists: Dr C Bouteloup, Dr N Farigon. Clinical Assistant: Sophia Sickout Argondo, Emilie Dumont. Nurse: Sandrine Rouvet. Caen Neurologists: Pr Fausto Viader, Dr Mathilde Lefilliatre, Dr Philippe Mouton, Dr A Mondou. Biologists: Pr Stephane Allouche. Clinical Assistant: Rachida Bari-Makouri. Saint-Brieuc Neurologists: Dr Ivan Kolev, Dr Morgane Pihan. Pneumologists: Dr Helene Le Ho. Neuroradiologists: Bertrand Catroux. Neuropsychologists: Maela Castel, Marine Rigal. Clinical Assistant: Catherine Bellot, Maelle Vomscheid, Marie-Cécile Hervé, Marie-Pierre Duban. Angers Neurologists: Dr Anne Vieillart, Dr Julien Cassereau, Dr Philippe Codron, Dr Vivien Pautot. Pneumologists: Dr Nicole Meslier, Dr Wojciech Trzepizur. Neuroradiologists: JY Tanguy. Neuropsychologists: Pr Philippe Allain, Cecile Thiery. Biologists: Pascal. Reynier. Physical therapists: Tiphaine Barbe, Vialle-Soubranne. Nutritionists: Nathalie Vienne. Clinical Assistant: Audrey Olivier, Jeanne Miller, Marie Bost. Nusre: Fournier. CATI (MRI acquisition management, preprocessing and data management): . David Gay, Robin Bonicel, Fouzia El Mountassir, Clara Fischer, Jean-François Mangin, Marie Chupin, Yann Cointepas. CRB of Lille (Center of Biological Resources): Bertrand Accart, Patrick Gelé, Florine Fievet, Matthieu Chabel, Virginie Derenaucourt, Loïc Facon, Yanick Tchantchou Njosse, Michael Hisbergues, Deplanque. Data management of Lille: Alain Duhamel, Lynda Djemmane, Florence Duflot, Hajar Chouiki. ARSLA CSV (Comité Scientifique et de Valorisation) and CSP (Comité de Suivi et de Pilotage): Christine Tabuenca, Marie-France Cazalère, Philippe Couratier, William Camu, Philippe Corcia, Claude Desnuelle, Maxime Caillier, Véronique Danel, Caroline Morerau, Victor Laugeais, Amelie Lecocq, Nathalie Potin, Marie Frisch, Marie Léon, David Devos, François Salachas, Pierre-Francois Pradat, Lucette Lacomblez, Jean-Philippe Camdessanché, Sharam Attarian, Timothée Langlet, Hélène Blasco, Luc Dupuis, Mathilde Bon, Emilien Bernard, Julien Cassereau, Marie-Hélène Soriani, Cedric Raoul, Sylvain Lehman, Sabine Turgeman, Valérie Goutines.
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This study was conducted in accordance with good clinical practise guidelines and local regulations. All participants gave written informed consent prior to participation in the study. The study was approved by the CPP Nord Ouest-IV Ethical Committee (ID-RCB 2013-A00969-36).
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Khamaysa, M., Lefort, M., Pélégrini-Issac, M. et al. Comparison of spinal magnetic resonance imaging and classical clinical factors in predicting motor capacity in amyotrophic lateral sclerosis. J Neurol 270, 3885–3895 (2023). https://doi.org/10.1007/s00415-023-11727-w
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DOI: https://doi.org/10.1007/s00415-023-11727-w