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May 2018; 5 (3) ArticleOpen Access

Microglial activation, white matter tract damage, and disability in MS

Eero Rissanen, Jouni Tuisku, Tero Vahlberg, Marcus Sucksdorff, Teemu Paavilainen, Riitta Parkkola, Johanna Rokka, Alexander Gerhard, Rainer Hinz, Peter S. Talbot, Juha O. Rinne, Laura Airas
First published March 6, 2018, DOI: https://doi.org/10.1212/NXI.0000000000000443
Eero Rissanen
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Jouni Tuisku
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Tero Vahlberg
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Marcus Sucksdorff
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Teemu Paavilainen
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Riitta Parkkola
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Johanna Rokka
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Alexander Gerhard
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Rainer Hinz
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Peter S. Talbot
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Juha O. Rinne
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Laura Airas
From the Turku PET Centre (E.R., J.T., M.S., J.R., J.O.R.), Division of Clinical Neurosciences (E.R., M.S., J.O.R., L.A.), Department of Biostatistics (T.V.), and Medical Imaging Centre of Southwest Finland (T.P., R.P.), Turku University Hospital and University of Turku, Finland; Division of Neuroscience and Experimental Psychology (A.G.), University of Manchester, United Kingdom; Department of Nuclear Medicine and Geriatric Medicine (A.G.), University Hospital Essen, Germany; and Wolfson Molecular Imaging Centre (R.H., P.S.T.), University of Manchester, United Kingdom.
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Citation
Microglial activation, white matter tract damage, and disability in MS
Eero Rissanen, Jouni Tuisku, Tero Vahlberg, Marcus Sucksdorff, Teemu Paavilainen, Riitta Parkkola, Johanna Rokka, Alexander Gerhard, Rainer Hinz, Peter S. Talbot, Juha O. Rinne, Laura Airas
Neurol Neuroimmunol Neuroinflamm May 2018, 5 (3) e443; DOI: 10.1212/NXI.0000000000000443

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    Figure 1 Illustration of white matter– and lesion-associated regions of interest (ROIs)

    The images are from a 25-year-old female patient with relapsing-remitting MS and an Expanded Disability Status Scale score of 1.0. (A) Axial view of gadolinium-enhanced 3DT1 MRI showing T1-hypointense white matter lesions. (B) Respective MRI with overlaid ROIs of T1-hypointense lesions (red), perilesional areas with 0-3 mm (brown) and 3-6 mm (yellow) radiuses, and normal-appearing white matter (green). Note that some of the perilesional ROIs visible in this slice are not associated with T1-hypointense lesions, but are due to larger perilesional ROIs associated with T1-hypointense lesion cores in adjacent sections. The gray matter areas have been masked out from all the lesion-associated ROIs for all analyses.

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    Figure 2 Region of interest (ROI)-specific [11C](R)-PK11195 binding in patients with relapsing-remitting MS (RRMS), patients with secondary progressive MS (SPMS), and controls

    Radioligand binding by group among healthy controls (HC, n = 17), patients with RRMS (n = 10), and patients with SPMS (n = 10) in non–lesion-associated ROIs (A), gadolinium-negative lesion-associated ROIs (B), and gadolinium-positive lesion-associated ROIs (C). Each boxplot represents the group median, 1st and 3rd quartiles, minimum and maximum, and outliers (black dots) of distribution volume ratio (DVR) values in each ROI. NAWM = normal-appearing white matter; T1 Gd− = T1-hypointense, gadolinium-negative lesion ROI (including all T1 Gd− lesions); Gd− 0–3 mm rim = perilesional circular ROI 0–3 mm from the edge of gadolinium-negative lesions; Gd− 3–6 mm rim = perilesional circular ROI 3–6 mm from the edge of gadolinium-negative lesions; T1 Gd+ = T1-hypointense, gadolinium-positive lesion ROI (including all T1 Gd+ lesions); Gd+ 0–3 mm rim = perilesional circular ROI 0–3 mm from the edge of gadolinium-positive lesions; Gd+ 3–6 mm rim = perilesional circular ROI 3–6 mm from the edge of gadolinium-positive lesions. *Analysis of , age as a covariate, p < 0.05. #Repeated-measures analysis of variance (ANOVA), p < 0.05. ##Repeated-measures ANOVA, p < 0.001.

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    Figure 3 Associations of [11C](R)-PK11195 binding to disability and diffusion tensor imaging (DTI) changes in patients with MS

    Region of interest–specific binding of [11C](R)-PK11195 measured as the distribution volume ratio (DVR) in the normal-appearing white matter (NAWM) plotted with (A) Expanded Disability Status Scale (EDSS), (B) MS severity score (MSSS), (C) mean fractional anisotropy (FA) in the NAWM, and (D) the DVR in the thalami plotted with mean FA in the NAWM in the pooled MS patient group. The correlations are visualized with linear regression lines corresponding to the results from repeated-measures analysis of covariance (rm ANCOVA) reported in tables e-1 and e-3 (links.lww.com/NXI/A37). SPMS = secondary progressive MS; RRMS = relapsing-remitting MS.

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    Figure 4 Correlation of age with [11C](R)-PK11195 binding in the normal-appearing white matter (NAWM) and thalami

    (A and C) Patients with MS, n = 20. (B and D) Controls, n = 17. The correlations are visualized with linear regression lines corresponding to the results from repeated-measures analysis of covariance (rm ANCOVA). SPMS = secondary progressive MS; RRMS = relapsing-remitting MS; HC = healthy control.

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