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January 03, 2023; 100 (1) Research Article

In Vivo 2-Hydroxyglutarate Monitoring With Edited MR Spectroscopy for the Follow-up of IDH-Mutant Diffuse Gliomas

The IDASPE Prospective Study

View ORCID ProfileAnna Luisa Di Stefano, Lucia Nichelli, View ORCID ProfileGiulia Berzero, Romain Valabregue, Mehdi Touat, Laurent Capelle, Clément Pontoizeau, Franck Bielle, Julie Lerond, Marine Giry, Chiara Villa, Bertrand Baussart, Caroline Dehais, Damien Galanaud, Capucine Baldini, Julien Savatovsky, Frédéric Dhermain, Dinesh K. Deelchand, Chris Ottolenghi, Stéphane Lehéricy, Małgorzata Marjańska, Francesca Branzoli, Marc Sanson
First published September 30, 2022, DOI: https://doi.org/10.1212/WNL.0000000000201137
Anna Luisa Di Stefano
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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  • ORCID record for Anna Luisa Di Stefano
Lucia Nichelli
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Giulia Berzero
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Romain Valabregue
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Mehdi Touat
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Laurent Capelle
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Clément Pontoizeau
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Franck Bielle
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Julie Lerond
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Marine Giry
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Chiara Villa
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Bertrand Baussart
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Caroline Dehais
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Damien Galanaud
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Capucine Baldini
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Julien Savatovsky
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Frédéric Dhermain
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Dinesh K. Deelchand
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Chris Ottolenghi
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Stéphane Lehéricy
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Małgorzata Marjańska
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Francesca Branzoli
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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Marc Sanson
From the Sorbonne Université (A.L.D.S.,M.D.P.D., L.N., M.D.P.D., J.L., M.G., S.L., Francesca Branzoli), Inserm, CNRS, Paris Brain Institute—Institut du Cerveau (ICM), Paris, France. Equipe labellisée LNCC; Service de Neurologie 2-Mazarin (A.L.D.S.,M.D.P.D., M.D.P.D., C.D.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Neuroradiologie Diagnostique et Interventionnelle (L.N., D.G., S.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Neurology Unit (G.B.), IRCCS San Raffaele Scientific Institute, Milan, Italy; Centre de NeuroImagerie de Recherche (CENIR) (R.V., S.L., Francesca Branzoli), Institut du Cerveau (ICM), Paris, France; Service de Neurochirurgie (L.C., B.B.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Service de Biochimie Métabolique (C.P.), AP-HP, Hôpital Necker, Paris, France; Laboratoire R Escourolle (J.L.), AP-HP, Hôpitaux Universitaires La Pitié Salpêtrière - Charles Foix, Paris, France; Drug Development Department (DITEP) (C.B.), Gustave Roussy, Villejuif, France; Service de Radiologie (J.S.), Fondation Ophtalmologique Adolphe de Rothschild, Paris, France; Radiotherapy Department (F.D.), Gustave Roussy University Hospital, Villejuif, Cedex, France; Center for Magnetic Resonance Research (D.K.D., M.M.), Department of Radiology, Minneapolis, MN; and OncoNeuroTek Tumor Bank (M.D.P.D.), Institut du Cerveau et de la Moelle épinière (ICM), Paris, France.
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In Vivo 2-Hydroxyglutarate Monitoring With Edited MR Spectroscopy for the Follow-up of IDH-Mutant Diffuse Gliomas
The IDASPE Prospective Study
Anna Luisa Di Stefano, Lucia Nichelli, Giulia Berzero, Romain Valabregue, Mehdi Touat, Laurent Capelle, Clément Pontoizeau, Franck Bielle, Julie Lerond, Marine Giry, Chiara Villa, Bertrand Baussart, Caroline Dehais, Damien Galanaud, Capucine Baldini, Julien Savatovsky, Frédéric Dhermain, Dinesh K. Deelchand, Chris Ottolenghi, Stéphane Lehéricy, Małgorzata Marjańska, Francesca Branzoli, Marc Sanson
Neurology Jan 2023, 100 (1) e94-e106; DOI: 10.1212/WNL.0000000000201137

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Abstract

Background and Objectives D-2-hydroxyglutarate (2HG) characterizes IDH-mutant gliomas and can be detected and quantified with edited MRS (MEGA-PRESS). In this study, we investigated the clinical, radiologic, and molecular parameters affecting 2HG levels.

Methods MEGA-PRESS data were acquired in 71 patients with glioma (24 untreated, 47 treated) on a 3 T system. Eighteen patients were followed during cytotoxic (n = 12) or targeted (n = 6) therapy. 2HG was measured in tumor samples using gas chromatography coupled to mass spectrometry (GCMS).

Results MEGA-PRESS detected 2HG with a sensitivity of 95% in untreated patients and 62% in treated patients. Sensitivity depended on tumor volume (>27 cm3; p = 0.02), voxel coverage (>75%; p = 0.002), and expansive presentation (defined by equal size of T1 and FLAIR abnormalities, p = 0.04). 2HG levels were positively correlated with IDH-mutant allelic fraction (p = 0.03) and total choline levels (p < 0.001) and were higher in IDH2-mutant compared with IDH1R132H-mutant and non–R132H IDH1-mutant patients (p = 0.002). In patients receiving IDH inhibitors, 2HG levels decreased within a few days, demonstrating the on-target effect of the drug, but 2HG level decrease did not predict tumor response. Patients receiving cytotoxic treatments showed a slower decrease in 2HG levels, consistent with tumor response and occurring before any tumor volume change on conventional MRI. At progression, 1p/19q codeleted gliomas, but not the non-codeleted, showed detectable in vivo 2HG levels, pointing out to different modes of progression characterizing these 2 entities.

Discussion MEGA-PRESS edited MRS allows in vivo monitoring of 2-hydroxyglutarate, confirming efficacy of IDH inhibition and suggests different patterns of tumor progression in astrocytomas compared with oligodendrogliomas.

Glossary

2HG=
2-hydroxyglutarate;
CRLB=
Cramer Rao lower bounds;
IDH=
isocitrate dehydrogenase;
MRS=
magnetic resonance spectroscopy;
RT=
radiotherapy;
VOI=
volume of interest

Footnotes

  • ↵* These authors contributed equally to the manuscript.

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Submitted and externally peer reviewed. The handling editor was Rebecca Burch, MD.

  • Received November 6, 2021.
  • Accepted in final form July 5, 2022.
  • © 2022 American Academy of Neurology
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