Grey Matter Atrophy and its Relationship with White Matter Lesions in Patients with Myelin Oligodendrocyte Glycoprotein Antibody‐associated Disease, Aquaporin‐4 Antibody‐Positive Neuromyelitis Optica Spectrum Disorder, and Multiple Sclerosis-Reference-Cited by-同舟云学术

Grey Matter Atrophy and its Relationship with White Matter Lesions in Patients with Myelin Oligodendrocyte Glycoprotein Antibody‐associated Disease, Aquaporin‐4 Antibody‐Positive Neuromyelitis Optica Spectrum Disorder, and Multiple Sclerosis

Published:2024-05-23 Issue:2 Volume:96 Page:276-288
ISSN:0364-5134
Container-title:Annals of Neurology
language:en
Short-container-title:Annals of Neurology

Author:

Cortese Rosa¹²^ORCID,Battaglini Marco¹³,Prados Ferran²⁴⁵,Gentile Giordano¹³,Luchetti Ludovico¹³,Bianchi Alessia²^ORCID,Haider Lukas²^ORCID,Jacob Anu⁶⁷,Palace Jacqueline⁸,Messina Silvia⁸^ORCID,Paul Friedemann⁹^ORCID,Marignier Romain¹⁰^ORCID,Durand‐Dubief Françoise¹⁰,de Medeiros Rimkus Carolina¹¹,Apostolos Pereira Samira Luisa¹²,Sato Douglas Kazutoshi¹³^ORCID,Filippi Massimo¹⁴¹⁵¹⁶¹⁷¹⁸^ORCID,Rocca Maria Assunta¹⁴¹⁵¹⁸^ORCID,Cacciaguerra Laura¹⁴¹⁵,Rovira Àlex¹⁹^ORCID,Sastre‐Garriga Jaume²⁰^ORCID,Arrambide Georgina²⁰,Liu Yaou²¹^ORCID,Duan Yunyun²¹,Gasperini Claudio²²^ORCID,Tortorella Carla²²,Ruggieri Serena²³²⁴,Amato Maria Pia²⁵²⁶,Ulivelli Monica¹,Groppa Sergiu²⁷,Grothe Matthias²⁸^ORCID,Llufriu Sara²⁹^ORCID,Sepulveda Maria²⁹,Lukas Carsten³⁰³¹^ORCID,Bellenberg Barbara³⁰,Schneider Ruth³⁰³¹,Sowa Piotr³²,Celius Elisabeth G.³³,Pröbstel Anne‐Katrin³⁴^ORCID,Granziera Cristina³⁴³⁵,Yaldizli Özgür³⁴,Müller Jannis³⁴³⁵^ORCID,Stankoff Bruno³⁶^ORCID,Bodini Benedetta³⁶,Barkhof Frederik⁴³⁷,Ciccarelli Olga²³⁸,De Stefano Nicola¹,

Affiliation:

1. Department of Medicine, Surgery and Neuroscience University of Siena Siena Italy

2. Queen Square MS Center, Department of Neuroinflammation, UCL Queen Square Institute of Neurology, Faculty of Brain Sciences University College London London UK

3. SIENA imaging SRL Siena Italy

4. Center for Medical Imaging Computing, Medical Physics, and Biomedical Engineering UCL London UK

5. E‐Health Center University Oberta de Catalunya Barcelona Spain

6. NMO Clinical Service at the Walton Centre Liverpool UK

7. Department of Neurology Cleveland Clinic Abu Dhabi UAE

8. Department of Clinical Neurology John Radcliffe Hospital Oxford UK

9. Experimental and Clinical Research Center, Max Delbrueck Center for Molecular Medicine and Charité‐Universitaetsmedizin Berlin Berlin Germany

10. Department of Neurology, Multiple Sclerosis, Myelin Disorders, and Neuro‐inflammation, Pierre Wertheimer Neurological Hospital, Hospices Civils de Lyon Lyon France

11. Department of Radiology and Oncology, Faculty of Medicine University of São Paulo (FMUSP) São Paulo Brazil

12. Department of Neurology, Faculty of Medicine University of São Paulo (FMUSP) São Paulo Brazil

13. Pontifical Catholic University of Rio Grande do Sul (PUCRS), School of Medicine Porto Alegre Brazil

14. Neuroimaging Research Unit, Division of Neuroscience IRCCS San Raffaele Scientific Institute Milan Italy

15. Neurology Unit, IRCCS San Raffaele Scientific Institute Milan Italy

16. Neurorehabilitation Unit, IRCCS San Raffaele Scientific Institute Milan Italy

17. Neurophysiology Service, IRCCS San Raffaele Scientific Institute Milan Italy

18. Vita‐Salute San Raffaele University Milan Italy

19. Section of Neuroradiology, Department of Radiology Hospital Universitari Vall d'Hebron, Universitat Autònoma de Barcelona Barcelona Spain

20. Multiple Sclerosis Centre of Catalonia (Cemcat), Department of Neurology, Hospital Universitari Vall d'Hebron, Universitat Autònoma de Barcelona Barcelona Spain

21. Department of Radiology Beijing Tiantan Hospital, Capital Medical University Beijing China

22. Department of Neurosciences S. Camillo‐Forlanini Hospital Rome Italy

23. Department of Human Neurosciences Sapienza University of Rome Rome Italy

24. Neuroimmunology Unit, IRCSS Fondazione Santa Lucia Rome Italy

25. Department Neurofarba University of Florence Florence Italy

26. IRCCS Don Carlo Gnocchi Foundation Florence Italy

27. Department of Neurology University Medical Center of the Johannes Gutenberg University Mainz Mainz Germany

28. Department of Neurology University Medicine of Greifswald Greifswald Germany

29. Service of Neurology, Laboratory of Advanced Imaging in Neuroimmunological Diseases Center of Neuroimmunology, Hospital Clínic of Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), and Universitat de Barcelona Barcelona Spain

30. Institute of Neuroradiology, St. Josef Hospital, Ruhr University Bochum Bochum Germany

31. Department of Neurology St. Josef Hospital, Ruhr University Bochum Bochum Germany

32. Division of Radiology and Nuclear Medicine Oslo University Hospital Oslo Norway

33. Department of Neurology Oslo University Hospital and Faculty of Medicine, University of Oslo Oslo Norway

34. Department of Neurology, Biomedicine and Clinical Research, and Research Center for Clinical Neuroimmunology and Neuroscience Basel University Hospital and University of Basel Basel Switzerland

35. Translational Imaging in Neurology (ThINk) Basel, Department of Biomedical Engineering University Hospital Basel and University of Basel Basel Switzerland

36. Sorbonne University, Paris Brain Institute, ICM, Pitié Salpêtrière Hospital Paris France

37. Radiology & Nuclear medicine, VU University Medical Center Amsterdam The Netherlands

38. National Institute for Health Research (NIHR) University College London Hospitals (UCLH) Biomedical Research Center London UK

Abstract

ObjectiveTo evaluate: (1) the distribution of gray matter (GM) atrophy in myelin oligodendrocyte glycoprotein antibody‐associated disease (MOGAD), aquaporin‐4 antibody‐positive neuromyelitis optica spectrum disorder (AQP4+NMOSD), and relapsing–remitting multiple sclerosis (RRMS); and (2) the relationship between GM volumes and white matter lesions in various brain regions within each disease.MethodsA retrospective, multicenter analysis of magnetic resonance imaging data included patients with MOGAD/AQP4+NMOSD/RRMS in non‐acute disease stage. Voxel‐wise analyses and general linear models were used to evaluate the relevance of regional GM atrophy. For significant results (p < 0.05), volumes of atrophic areas are reported.ResultsWe studied 135 MOGAD patients, 135 AQP4+NMOSD, 175 RRMS, and 144 healthy controls (HC). Compared with HC, MOGAD showed lower GM volumes in the temporal lobes, deep GM, insula, and cingulate cortex (75.79 cm3); AQP4+NMOSD in the occipital cortex (32.83 cm3); and RRMS diffusely in the GM (260.61 cm3). MOGAD showed more pronounced temporal cortex atrophy than RRMS (6.71 cm3), whereas AQP4+NMOSD displayed greater occipital cortex atrophy than RRMS (19.82 cm3). RRMS demonstrated more pronounced deep GM atrophy in comparison with MOGAD (27.90 cm3) and AQP4+NMOSD (47.04 cm3). In MOGAD, higher periventricular and cortical/juxtacortical lesions were linked to reduced temporal cortex, deep GM, and insula volumes. In RRMS, the diffuse GM atrophy was associated with lesions in all locations. AQP4+NMOSD showed no lesion/GM volume correlation.InterpretationGM atrophy is more widespread in RRMS compared with the other two conditions. MOGAD primarily affects the temporal cortex, whereas AQP4+NMOSD mainly involves the occipital cortex. In MOGAD and RRMS, lesion‐related tract degeneration is associated with atrophy, but this link is absent in AQP4+NMOSD. ANN NEUROL 2024;96:276–288

Publisher

Wiley

Link

https://onlinelibrary.wiley.com/doi/pdf/10.1002/ana.26951

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