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November 2022; 9 (6) Research ArticleOpen Access

Imaging Characteristics of Choroid Plexuses in Presymptomatic Multiple Sclerosis

A Retrospective Study

Vito A.G. Ricigliano, Céline Louapre, Emilie Poirion, Annalisa Colombi, Arya Yazdan Panah, Andrea Lazzarotto, Emanuele Morena, Elodie Martin, Michel Bottlaender, Benedetta Bodini, Danielle Seilhean, Bruno Stankoff
First published October 13, 2022, DOI: https://doi.org/10.1212/NXI.0000000000200026
Vito A.G. Ricigliano
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Céline Louapre
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Emilie Poirion
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Annalisa Colombi
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Arya Yazdan Panah
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Andrea Lazzarotto
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Emanuele Morena
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Elodie Martin
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Michel Bottlaender
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Benedetta Bodini
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Danielle Seilhean
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Bruno Stankoff
From the Sorbonne Université (V.A.G.R., C.L., E.P., A.C., A.Y.P., A.L., Emanuele Morena, Elodie Martin, B.B., D.S., B.S.), Paris Brain Institute, ICM, CNRS, Inserm; Neurology Department (V.A.G.R., A.L., B.B., B.S.), St Antoine Hospital, APHP-Sorbonne, Paris; Neurology Department (C.L.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris; Service D'Imagerie Médicale (E.P.), Hôpital Fondation Adolphe de Rothschild, Paris; Université Paris-Saclay (M.B.), CEA, CNRS, Inserm, BioMaps, Service Hospitalier Frédéric Joliot, Orsay; and Neuropathology Department (D.S.), Pitié-Salpêtrière Hospital, APHP-Sorbonne, Paris, France.
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Full PDF
Citation
Imaging Characteristics of Choroid Plexuses in Presymptomatic Multiple Sclerosis
A Retrospective Study
Vito A.G. Ricigliano, Céline Louapre, Emilie Poirion, Annalisa Colombi, Arya Yazdan Panah, Andrea Lazzarotto, Emanuele Morena, Elodie Martin, Michel Bottlaender, Benedetta Bodini, Danielle Seilhean, Bruno Stankoff
Neurol Neuroimmunol Neuroinflamm Nov 2022, 9 (6) e200026; DOI: 10.1212/NXI.0000000000200026

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    Figure 1 Enlarged CPs in Presymptomatic MS

    (A) Unenhanced 3D T1-weighted magnetization-prepared rapid gradient echo (MPRAGE) images showing the segmentation of the left and right CP (outlined in red) in axial (top) and coronal (bottom) planes in a patient with presymptomatic MS. (B) Box plots showing significantly higher CP volume in the whole presymptomatic MS group vs HCs and no difference compared with MS. CP volume was normalized according to TIV. Note that the dot corresponding to the volume of the presymptomatic case further examined in the PET part of this study is colored in red. Box represents the interquartile range and median, whereas whiskers represent minimum and maximum values in data. The p value corresponds to that of the multivariable linear regression model. (C–D) Graphical illustration of the distribution of normalized CP volume in HCs vs the single presymptomatic woman (C) and in MS vs the single presymptomatic woman (D) from the Crawford-Howell test. Note that the presence of a distribution for a single case value is based on the assumptions of the test performed and depends on the statistics of the reference cohort. CP = choroid plexus; HCs = healthy controls; MS = multiple sclerosis; TIV = total intracranial volume.

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    Figure 2 Higher 18F-DPA-714 Uptake in the CPs of Presymptomatic MS

    (A) Axial 18F-DPA-714 SUV60-90 map registered onto the 3D T1-weighted magnetization-prepared rapid gradient echo (MPRAGE) image of the presymptomatic MS case, with the corresponding color bar (left) and magnification on the CP of the right lateral ventricle (right). (B, C) Examples of axial 18F-DPA-714 SUV60-90 maps registered onto the 3D T1-weighted MPRAGE images from 2 controls (B) and 2 patients with RRMS (C). (D, E) Graphical illustration of the distribution of CP 18F-DPA-714 SUV60-90 in HCs vs the presymptomatic woman (D) and in MS vs the presymptomatic woman (E) from the Crawford-Howell test. The presence of a distribution for a single case value is based on the assumptions of the test performed and depends on the statistics of the reference cohort. CP = choroid plexus; HCs = healthy controls; MS = multiple sclerosis; SUV60-90 = standardized uptake value between 60 and 90 minutes of acquisition; TIV = total intracranial volume.

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    Figure 3 TSPO+/CD163+ Macrophages Are Found in MS CPs

    (A, B) Excess of CD163+ macrophages (mouse monoclonal antibody, Cell Marque®; brown, arrows) in a PPMS case (A) compared with a healthy control (B). (C, F) TSPO (monoclonal rabbit antibody, Abcam®; brown) is highly expressed in epithelial cells (arrows) of choroid plexuses in both MS (C: PPMS and E: SPMS) and controls (D: HCs and F: epilepsy control). CD163+ (red) and TSPO+ (brown) perivascular macrophages (arrowheads) are found in MS (C, E), but not in controls (D, F). Scale bars = 40 µm (A, B) and 20 µm (C–F). HCs = healthy controls; MS = multiple sclerosis; PPMS = primary progressive MS; SPMS = secondary progressive MS; TSPO = translocator protein.

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