November 12, 2019; 93 (20) Article
Clinically relevant cranio-caudal patterns of cervical cord atrophy evolution in MS
View ORCID ProfileMaria A. Rocca, Paola Valsasina, Alessandro Meani, Claudio Gobbi, Chiara Zecca, Àlex Rovira, Xavier Montalban, Hugh Kearney, Olga Ciccarelli, Lucy Matthews, Jacqueline Palace, Antonio Gallo, Alvino Bisecco, Achim Gass, Philipp Eisele, Carsten Lukas, Barbara Bellenberg, View ORCID ProfileFrederik Barkhof, Hugo Vrenken, View ORCID ProfilePaolo Preziosa, Giancarlo Comi, Massimo Filippi, for the MAGNIMS Study Group
First published October 14, 2019, DOI: https://doi.org/10.1212/WNL.0000000000008466
Maria A. Rocca
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Paola Valsasina
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Alessandro Meani
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Claudio Gobbi
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Chiara Zecca
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Àlex Rovira
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Xavier Montalban
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Hugh Kearney
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Olga Ciccarelli
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Lucy Matthews
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Jacqueline Palace
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Antonio Gallo
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Alvino Bisecco
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Achim Gass
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Philipp Eisele
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Carsten Lukas
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Barbara Bellenberg
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Frederik Barkhof
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Hugo Vrenken
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Paolo Preziosa
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Giancarlo Comi
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Massimo Filippi
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
From the Neuroimaging Research Unit (M.A.R., P.V., A.M., P.P., M.F.) and Neurology Unit (M.A.R., P.P., G.C., M.F.), Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy; Department of Neurology (C.G., C.Z.), Neurocenter of Southern Switzerland, Regional Hospital Lugano (EOC), Lugano; Faculty of Biomedical Sciences (C.G., C.Z.), Università della Svizzera Italiana, Lugano, Switzerland; Section of Neuroradiology and MRI Unit, Department of Radiology (A.R.), and Department of Neurology/Neuroimmunology (X.M.), Multiple Sclerosis Centre of Catalonia, Hospital Universitari Vall d'Hebron, Barcelona, Spain; NMR Research Unit (H.K., O.C.), Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, London; Nuffield Department of Clinical Neurosciences (L.M., J.P.), University of Oxford, UK; Department of Advanced Medical and Surgical Sciences, and 3T MRI Center, (A.G., A.B.), University of Campania “Luigi Vanvitelli,” Naples, Italy; Department of Neurology (A.G., P.E.), Universitätsmedizin Mannheim, University of Heidelberg, Germany; Department of Radiology and Nuclear Medicine (C.L., B.B.) and Institute of Neuroradiology (C.L., B.B.), St. Josef Hospital, Ruhr-University Bochum, Germany; Department of Radiology and Nuclear Medicine (F.B., H.V.), MS Center Amsterdam, Amsterdam Neuroscience, Amsterdam UMC, location VUmc, the Netherlands; Institutes of Neurology and Healthcare Engineering (F.B.), University College London, UK; and Vita-Salute San Raffaele University (P.P., G.C., M.F.), Milan, Italy.
Clinically relevant cranio-caudal patterns of cervical cord atrophy evolution in MS
Maria A. Rocca, Paola Valsasina, Alessandro Meani, Claudio Gobbi, Chiara Zecca, Àlex Rovira, Xavier Montalban, Hugh Kearney, Olga Ciccarelli, Lucy Matthews, Jacqueline Palace, Antonio Gallo, Alvino Bisecco, Achim Gass, Philipp Eisele, Carsten Lukas, Barbara Bellenberg, Frederik Barkhof, Hugo Vrenken, Paolo Preziosa, Giancarlo Comi, Massimo Filippi, for the MAGNIMS Study Group
Neurology Nov 2019, 93 (20) e1852-e1866; DOI: 10.1212/WNL.0000000000008466
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Abstract
Objective To characterize the distribution and regional evolution of cervical cord atrophy in patients with multiple sclerosis (MS) in a multicenter dataset.
Methods MRI and clinical evaluations were acquired from 179 controls and 435 patients (35 clinically isolated syndromes [CIS], 259 relapsing-remitting multiple sclerosis [RRMS], 99 secondary progressive multiple sclerosis [SPMS], and 42 primary progressive multiple sclerosis [PPMS]). Sixty-nine controls and 178 patients underwent a 1-year MRI and clinical follow-up. Patients were classified as clinically stable/worsened according to their disability change. Longitudinal changes of cord atrophy were investigated with linear mixed-effect models. Sample size calculations were performed using age-, sex- and site-adjusted annualized percentage normalized cord cross-sectional area (CSAn) changes.
Results Baseline CSAn was lower in patients with MS vs controls (p < 0.001), but not different between controls and patients with CIS or between patients with early RRMS (disease duration ≤5 years) and patients with CIS. Patients with late RRMS (disease duration >5 years) showed significant cord atrophy vs patients with early RRMS (p = 0.02). Patients with progressive MS had decreased CSAn (p < 0.001) vs patients with RRMS. Atrophy was located between C1/C2 and C5 in patients with RRMS vs patients with CIS, and widespread along the cord in patients with progressive MS vs patients with RRMS, with an additional C5/C6 involvement in patients with SPMS vs patients with PPMS. At follow-up, CSAn decreased in all phenotypes (p < 0.001), except CIS. Cord atrophy rates were highest in patients with early RRMS and clinically worsened patients, who had a more widespread cord involvement than stable patients. The sample size per arm required to detect a 50% treatment effect was 118 for patients with early RRMS.
Conclusions Cord atrophy increased in MS during 1 year, except for CIS. Faster atrophy contributed to explain clinical worsening.
Glossary
- AS=
- active surface;
- CIS=
- clinically isolated syndrome;
- CSA=
- cross-sectional area;
- CSAn=
- normalized cross-sectional area;
- DE=
- dual echo;
- DMT=
- disease-modifying treatments;
- EDSS=
- Expanded Disability Status Scale;
- FLAIR=
- fluid-attenuated inversion recovery;
- FSE=
- fast spin-echo;
- GM=
- gray matter;
- HC=
- healthy controls;
- ICC=
- intraclass correlation coefficient;
- LV=
- lesion volumes;
- MS=
- multiple sclerosis;
- NBV=
- normalized brain volume;
- NWMV=
- normalized white matter volume;
- PBVC=
- percentage brain volume change;
- PPMS=
- primary progressive multiple sclerosis;
- RRMS=
- relapsing-remitting multiple sclerosis;
- SPMS=
- secondary progressive multiple sclerosis;
- STIR=
- short-tau inversion recovery
Footnotes
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.
Coinvestigators are listed in the appendix 2 at the end of the article.
- Received November 7, 2018.
- Accepted in final form June 4, 2019.
- © 2019 American Academy of Neurology
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