MR Imaging Features of Critical Spinal Demyelinating Lesions Associated with Progressive Motor Impairment

B Mark Keegan; Steven A Messina; Dennis Hanson; David Holmes; Jon Camp; Elia Sechi; Shreya Nayak; Benan Barakat; Rowaid Ahmad; Jay Mandrekar; W Scott Harmsen; Orhun Kantarci; Brian G Weinshenker; Eoin P Flanagan

doi:10.3174/ajnr.A8304

MR Imaging Features of Critical Spinal Demyelinating Lesions Associated with Progressive Motor Impairment

AJNR Am J Neuroradiol. 2024 May 16. doi: 10.3174/ajnr.A8304. Online ahead of print.

Authors

B Mark Keegan¹, Steven A Messina², Dennis Hanson³, David Holmes³, Jon Camp³, Elia Sechi^{4

5}, Shreya Nayak^{4

6}, Benan Barakat^{4

7}, Rowaid Ahmad^{4

8}, Jay Mandrekar^{4

9}, W Scott Harmsen⁹, Orhun Kantarci⁴, Brian G Weinshenker^{4

10}, Eoin P Flanagan⁴

Affiliations

¹ From the Department of Neurology (B.M.K., E.S., S.N., B.B., R.A., J.M., O.K., B.G.W., E.P.F.), Center for Multiple Sclerosis and Autoimmune Neurology, Mayo Clinic, Rochester, Minnesota keegan.bmark@mayo.edu.
² Department of Radiology (S.A.M.), Mayo Clinic, Rochester, Minnesota.
³ Biomedical Imaging Resource (D. Hanson, D. Holmes, J.C.), Mayo Clinic, Rochester, Minnesota.
⁴ From the Department of Neurology (B.M.K., E.S., S.N., B.B., R.A., J.M., O.K., B.G.W., E.P.F.), Center for Multiple Sclerosis and Autoimmune Neurology, Mayo Clinic, Rochester, Minnesota.
⁵ Università degli Studi di Sassari (E.S.), Sassari, Italy.
⁶ St. Elizabeth Dearborn Hospital (S.N.), Lawrenceburg, Indiana.
⁷ Mercy St. Vincent Medical Center (B.B.), Toledo, Ohio.
⁸ University of Texas Medical Branch (R.A.), Galveston, Texas.
⁹ Quantitative Health Services (J.M., W.S.H,), Mayo Clinic, Rochester, Minnesota.
¹⁰ Department of Neurology (B.G.W.), University of Virginia Health, Charlottesville, Virginia.

PMID: 38754997
DOI: 10.3174/ajnr.A8304

Abstract

Background and purpose: Progressive MS is typically heralded by a myelopathic pattern of asymmetric progressive motor weakness. Focal individual "critical" demyelinating spinal cord lesions anatomically associated with progressive motor impairment may be a compelling explanation for this clinical presentation as described in progressive solitary sclerosis (single CNS demyelinating lesion), progressive demyelination with highly restricted MR imaging lesion burden (2-5 total CNS demyelinating lesions; progressive paucisclerotic MS), and progressive, exclusively unilateral hemi- or monoparetic MS (>5 CNS demyelinating progressive unilateral hemi- or monoparetic MS [PUHMS] lesions). Critical demyelinating lesions appear strikingly similar across these cohorts, and we describe their specific spinal cord MR imaging characteristics.

Materials and methods: We performed a retrospective, observational MR imaging study comparing spinal cord critical demyelinating lesions anatomically associated with progressive motor impairment with any additional "noncritical" (not anatomically associated with progressive motor impairment) spinal cord demyelinating lesions. All spinal cord MR images (302 cervical and 91 thoracic) were reviewed by an experienced neuroradiologist with final radiologic assessment on the most recent MR imaging. Anatomic association with clinical progressive motor impairment was confirmed independently by MS subspecialists.

Results: Ninety-one individuals (PUHMS, 37 [41%], progressive paucisclerosis 35 [38%], progressive solitary sclerosis 19 [21%]) with 91 critical and 98 noncritical spinal cord MR imaging demyelinating lesions were evaluated. MR imaging characteristics that favored critical spinal cord demyelinating lesions over noncritical lesions included moderate-to-severe, focal, lesion-associated spinal cord atrophy: 41/91 (45%) versus 0/98 (0%) (OR, 161.91; 9.43 to >999.9); lateral column axial location (OR, 10.43; 3.88-28.07); central region (OR, 3.23; 1.78-5.88); ventral column (OR, 2.98; 1.55-5.72); and larger lesion size of the axial width (OR, 2.01;1.49-2.72), transverse axial size (OR, 1.66; 1.36-2.01), or lesion area (OR, 1.14; 1.08-1.2). Multiple regression analysis revealed focal atrophy and lateral axial location as having the strongest association with critical demyelinating lesions.

Conclusions: Focal, lesion-associated atrophy, lateral column axial location, and larger lesion size are spinal cord MR imaging characteristics of critical demyelinating lesions. The presence of critical demyelinating lesions should be sought as these features may be associated with the development of progressive motor impairment in MS.