MRI Patterns Distinguish AQP4 Antibody Positive Neuromyelitis Optica Spectrum Disorder From Multiple Sclerosis

Laura Clarke; Simon Arnett; Wajih Bukhari; Elham Khalilidehkordi; Sofia Jimenez Sanchez; Cullen O'Gorman; Jing Sun; Kerri M Prain; Mark Woodhall; Roger Silvestrini; Christine S Bundell; David A Abernethy; Sandeep Bhuta; Stefan Blum; Mike Boggild; Karyn Boundy; Bruce J Brew; Wallace Brownlee; Helmut Butzkueven; William M Carroll; Cella Chen; Alan Coulthard; Russell C Dale; Chandi Das; Marzena J Fabis-Pedrini; David Gillis; Simon Hawke; Robert Heard; Andrew P D Henderson; Saman Heshmat; Suzanne Hodgkinson; Trevor J Kilpatrick; John King; Christopher Kneebone; Andrew J Kornberg; Jeannette Lechner-Scott; Ming-Wei Lin; Christopher Lynch; Richard A L Macdonell; Deborah F Mason; Pamela A McCombe; Jennifer Pereira; John D Pollard; Sudarshini Ramanathan; Stephen W Reddel; Cameron P Shaw; Judith M Spies; James Stankovich; Ian Sutton; Steve Vucic; Michael Walsh; Richard C Wong; Eppie M Yiu; Michael H Barnett; Allan G K Kermode; Mark P Marriott; John D E Parratt; Mark Slee; Bruce V Taylor; Ernest Willoughby; Fabienne Brilot; Angela Vincent; Patrick Waters; Simon A Broadley

doi:10.3389/fneur.2021.722237

MRI Patterns Distinguish AQP4 Antibody Positive Neuromyelitis Optica Spectrum Disorder From Multiple Sclerosis

Front Neurol. 2021 Sep 9:12:722237. doi: 10.3389/fneur.2021.722237. eCollection 2021.

Authors

Laura Clarke¹, Simon Arnett¹, Wajih Bukhari¹, Elham Khalilidehkordi¹, Sofia Jimenez Sanchez¹, Cullen O'Gorman¹, Jing Sun¹, Kerri M Prain², Mark Woodhall³, Roger Silvestrini⁴, Christine S Bundell⁵, David A Abernethy⁶, Sandeep Bhuta¹, Stefan Blum⁷, Mike Boggild⁸, Karyn Boundy⁹, Bruce J Brew¹⁰, Wallace Brownlee¹¹, Helmut Butzkueven¹², William M Carroll¹³, Cella Chen¹⁴, Alan Coulthard¹⁵, Russell C Dale¹⁶, Chandi Das¹⁷, Marzena J Fabis-Pedrini¹³, David Gillis¹⁵, Simon Hawke¹⁸, Robert Heard¹⁶, Andrew P D Henderson¹⁹, Saman Heshmat¹, Suzanne Hodgkinson²⁰, Trevor J Kilpatrick²¹, John King²², Christopher Kneebone²³, Andrew J Kornberg²⁴, Jeannette Lechner-Scott²⁵, Ming-Wei Lin¹⁸, Christopher Lynch²⁶, Richard A L Macdonell²⁷, Deborah F Mason²⁸, Pamela A McCombe²⁹, Jennifer Pereira²⁶, John D Pollard¹⁸, Sudarshini Ramanathan^{30

31}, Stephen W Reddel¹⁶, Cameron P Shaw³², Judith M Spies¹⁸, James Stankovich³³, Ian Sutton³⁴, Steve Vucic¹⁹, Michael Walsh⁷, Richard C Wong¹⁵, Eppie M Yiu²⁴, Michael H Barnett¹⁶, Allan G K Kermode¹³, Mark P Marriott¹², John D E Parratt¹⁸, Mark Slee⁹, Bruce V Taylor³³, Ernest Willoughby¹¹, Fabienne Brilot^{16

30}, Angela Vincent³, Patrick Waters³, Simon A Broadley^{1

35}

Affiliations

¹ Menzies Health Institute Queensland, Gold Coast, Griffith University, Southport, QLD, Australia.
² Department of Immunology, Pathology Queensland, Royal Brisbane and Women's Hospital, Herston, QLD, Australia.
³ Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom.
⁴ Department of Immunopathology, Westmead Hospital, Westmead, NSW, Australia.
⁵ School of Pathology and Laboratory Medicine, University of Western Australia, Nedlands, WA, Australia.
⁶ Department of Neurology, Wellington Hospital, Newtown, New Zealand.
⁷ Department of Neurology, Princess Alexandra Hospital, Woolloongabba, QLD, Australia.
⁸ Department of Neurology, Townsville Hospital, Douglas, QLD, Australia.
⁹ Department of Neurology, College of Medicine and Public Health, Flinders University, Bedford Park, SA, Australia.
¹⁰ Centre for Applied Medical Research, St. Vincent's Hospital, University of New South Wales, Darlinghurst, NSW, Australia.
¹¹ Department of Neurology, Auckland City Hospital, Grafton, New Zealand.
¹² Melbourne Brain Centre, Royal Melbourne Hospital, University of Melbourne, Parkville, VIC, Australia.
¹³ Centre for Neuromuscular and Neurological Disorders, Queen Elizabeth II Medical Centre, Perron Institute for Neurological and Translational Science, University of Western Australia, Nedlands, WA, Australia.
¹⁴ Department of Ophthalmology, Flinders Medical Centre, Flinders University, Bedford Park, SA, Australia.
¹⁵ School of Medicine, Royal Brisbane and Women's Hospital, University of Queensland, Herston, QLD, Australia.
¹⁶ Brain and Mind Centre, University of Sydney, Camperdown, NSW, Australia.
¹⁷ Department of Neurology, Canberra Hospital, Garran, ACT, Australia.
¹⁸ Sydney Medical School, Royal Prince Alfred Hospital, University of Sydney, Camperdown, NSW, Australia.
¹⁹ Department of Neurology, Westmead Hospital, Westmead, NSW, Australia.
²⁰ South Western Sydney Medical School, Liverpool Hospital, University of New South Wales, Liverpool, NSW, Australia.
²¹ Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC, Australia.
²² Department of Neurology, Royal Melbourne Hospital, Parkville, VIC, Australia.
²³ Department of Neurology, Royal Adelaide Hospital, Adelaide, SA, Australia.
²⁴ School of Paediatrics, Royal Children's Hospital, University of Melbourne, Parkville, VIC, Australia.
²⁵ Hunter Medical Research Institute, University of Newcastle, New Lambton Heights, NSW, Australia.
²⁶ School of Medicine, University of Auckland, Grafton, New Zealand.
²⁷ Department of Neurology, Austin Health, Heidelberg, VIC, Australia.
²⁸ Department of Neurology, Christchurch Hospital, Christchurch, New Zealand.
²⁹ Centre for Clinical Research, Royal Brisbane and Women's Hospital, University of Queensland, Herston, QLD, Australia.
³⁰ Neuroimmunology Group, Kids Neurosciences Centre, Children's Hospital at Westmead, University of Sydney, Westmead, NSW, Australia.
³¹ Department of Neurology, Concord Repatriation General Hospital, Concord, NSW, Australia.
³² School of Medicine, Deakin University, Waurn Ponds, VIC, Australia.
³³ Menzies Research Institute, University of Tasmania, Hobart, TAS, Australia.
³⁴ Department of Neurology, St. Vincent's Hospital, Darlinghurst, NSW, Australia.
³⁵ Department of Neurology, Gold Coast University Hospital, Southport, QLD, Australia.

Abstract

Neuromyelitis optica spectrum disorder (NMOSD) and multiple sclerosis (MS) are inflammatory diseases of the CNS. Overlap in the clinical and MRI features of NMOSD and MS means that distinguishing these conditions can be difficult. With the aim of evaluating the diagnostic utility of MRI features in distinguishing NMOSD from MS, we have conducted a cross-sectional analysis of imaging data and developed predictive models to distinguish the two conditions. NMOSD and MS MRI lesions were identified and defined through a literature search. Aquaporin-4 (AQP4) antibody positive NMOSD cases and age- and sex-matched MS cases were collected. MRI of orbits, brain and spine were reported by at least two blinded reviewers. MRI brain or spine was available for 166/168 (99%) of cases. Longitudinally extensive (OR = 203), "bright spotty" (OR = 93.8), whole (axial; OR = 57.8) or gadolinium (Gd) enhancing (OR = 28.6) spinal cord lesions, bilateral (OR = 31.3) or Gd-enhancing (OR = 15.4) optic nerve lesions, and nucleus tractus solitarius (OR = 19.2), periaqueductal (OR = 16.8) or hypothalamic (OR = 7.2) brain lesions were associated with NMOSD. Ovoid (OR = 0.029), Dawson's fingers (OR = 0.031), pyramidal corpus callosum (OR = 0.058), periventricular (OR = 0.136), temporal lobe (OR = 0.137) and T1 black holes (OR = 0.154) brain lesions were associated with MS. A score-based algorithm and a decision tree determined by machine learning accurately predicted more than 85% of both diagnoses using first available imaging alone. We have confirmed NMOSD and MS specific MRI features and combined these in predictive models that can accurately identify more than 85% of cases as either AQP4 seropositive NMOSD or MS.

Keywords: NMOSD; diagnosis; magnetic resonance imaging; multiple sclerosis; neuromyelitis optica.

Copyright © 2021 Clarke, Arnett, Bukhari, Khalilidehkordi, Jimenez Sanchez, O'Gorman, Sun, Prain, Woodhall, Silvestrini, Bundell, Abernethy, Bhuta, Blum, Boggild, Boundy, Brew, Brownlee, Butzkueven, Carroll, Chen, Coulthard, Dale, Das, Fabis-Pedrini, Gillis, Hawke, Heard, Henderson, Heshmat, Hodgkinson, Kilpatrick, King, Kneebone, Kornberg, Lechner-Scott, Lin, Lynch, Macdonell, Mason, McCombe, Pereira, Pollard, Ramanathan, Reddel, Shaw, Spies, Stankovich, Sutton, Vucic, Walsh, Wong, Yiu, Barnett, Kermode, Marriott, Parratt, Slee, Taylor, Willoughby, Brilot, Vincent, Waters and Broadley.