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April 07, 2015; 84 (14) Article

Differential patterns of spinal cord and brain atrophy in NMO and MS

Yaou Liu, Jinhui Wang, Marita Daams, Florian Weiler, Horst K. Hahn, Yunyun Duan, Jing Huang, Zhuoqiong Ren, Jing Ye, Huiqing Dong, Hugo Vrenken, Mike P. Wattjes, Fu-Dong Shi, Kuncheng Li, Frederik Barkhof
First published March 11, 2015, DOI: https://doi.org/10.1212/WNL.0000000000001441
Yaou Liu
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Jinhui Wang
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Marita Daams
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Florian Weiler
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Horst K. Hahn
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Yunyun Duan
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Jing Huang
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Zhuoqiong Ren
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Jing Ye
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Huiqing Dong
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Hugo Vrenken
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Mike P. Wattjes
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Fu-Dong Shi
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Kuncheng Li
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Frederik Barkhof
From the Departments of Radiology (Y.L., Y.D., J.H., Z.R., K.L.) and Neurology (J.Y., H.D.), Xuanwu Hospital, Capital Medical University, Beijing, China; the Department of Radiology and Nuclear Medicine, Neuroscience Campus Amsterdam (Y.L., M.D., H.V., M.P.W., F.B.), and the Department of Anatomy and Neurosciences, Section of Clinical Neuroscience (M.D.), VU University Medical Center, Amsterdam, the Netherlands; the Department of Neurology and Tianjin Neurological Institute (Y.L., F.-D.S.), Tianjin Medical University, General Hospital, China; the Center for Cognition and Brain Disorders (J.W.), Hangzhou Normal University; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments (J.W.), Hangzhou, China; and Fraunhofer MEVIS (F.W., H.K.H.), Institute for Medical Image Computing, Bremen, Germany.
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Citation
Differential patterns of spinal cord and brain atrophy in NMO and MS
Yaou Liu, Jinhui Wang, Marita Daams, Florian Weiler, Horst K. Hahn, Yunyun Duan, Jing Huang, Zhuoqiong Ren, Jing Ye, Huiqing Dong, Hugo Vrenken, Mike P. Wattjes, Fu-Dong Shi, Kuncheng Li, Frederik Barkhof
Neurology Apr 2015, 84 (14) 1465-1472; DOI: 10.1212/WNL.0000000000001441

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Abstract

Objective: To investigate spinal cord and brain atrophy in neuromyelitis optica (NMO), and its relationship with other MRI measurements and clinical disability, compared with patients with multiple sclerosis (MS) and healthy controls (HC).

Methods: We recruited 35 patients with NMO, 35 patients with MS, and 35 HC, who underwent both spinal cord and brain MRI. Mean upper cervical cord area (MUCCA), brain parenchymal fraction (BPF), gray matter fraction (GMF), white matter fraction (WMF), and spinal cord and brain lesion loads were measured and compared among groups. Multivariate associations between MUCCA and brain volume measurement and clinical variables were assessed by partial correlations and multiple linear regression.

Results: Patients with NMO showed smaller MUCCA than HC (p = 0.004), and patients with MS had a trend of smaller MUCCA compared to HC (p = 0.07), with no significant difference between the patient groups. Patients with NMO showed lower BPF than HC, and patients with MS had lower BPF and GMF than patients with NMO. In NMO, MUCCA was correlated with Expanded Disability Status Scale score (EDSS), number of relapses, and total spinal cord lesion length, while in MS, MUCCA was correlated with WMF and EDSS. MUCCA was the only independent variable for predicting clinical disability measured by EDSS in NMO (R2 = 0.55, p < 0.001) and MS (R2 = 0.17, p = 0.013).

Conclusion: NMO showed predominately spinal cord atrophy with mild brain atrophy, while MS demonstrated more brain atrophy, especially in the gray matter. MUCCA is the main MRI-derived parameter for explaining clinical disability in NMO and MS, and may serve as a potential biomarker for further clinical trials, especially in NMO.

GLOSSARY

AQP4=
aquaporin-4;
ARR=
annualized relapse rate;
BPF=
brain parenchymal fraction;
EDSS=
Expanded Disability Status Scale;
FA=
flip angle;
FLAIR=
fluid-attenuated inversion recovery;
GM=
gray matter;
GMF=
gray matter fraction;
HC=
healthy controls;
ICC=
intraclass correlation coefficient;
MPRAGE=
magnetization-prepared rapidly acquired gradient echo;
MS=
multiple sclerosis;
MUCCA=
mean upper cervical cord area;
NMO=
neuromyelitis optica;
RRMS=
relapsing-remitting multiple sclerosis;
T1BH=
T1 black hole;
T2LV=
T2 lesion volumes;
TIV=
total intracranial volume;
TE=
echo time;
TR=
repetition time;
WM=
white matter;
WMF=
white matter fraction

Footnotes

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

  • Supplemental data at Neurology.org

  • Received June 26, 2014.
  • Accepted in final form December 16, 2014.
  • © 2015 American Academy of Neurology
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