3,425
Views
2
CrossRef citations to date
0
Altmetric
Perspective

What is the potential of paramagnetic rim lesions as diagnostic indicators in multiple sclerosis?

, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 829-837 | Received 15 Jul 2022, Accepted 31 Oct 2022, Published online: 08 Nov 2022

References

  • Kuhlmann T, Ludwin S, Prat A, et al. An updated histological classification system for multiple sclerosis lesions. Acta Neuropathol. 2017 Jan;133(1):13–24.
  • Fischer MT, Wimmer I, Hoftberger R, et al. Disease-specific molecular events in cortical multiple sclerosis lesions. Brain. 2013 Jun;136(Pt 6):1799–1815.
  • Luchetti S, Fransen NL, van Eden CG, et al. Progressive multiple sclerosis patients show substantial lesion activity that correlates with clinical disease severity and sex: a retrospective autopsy cohort analysis. Acta Neuropathol. 2018 Apr;135(4):511–528.
  • Bagnato F, Hametner S, Yao B, et al. Tracking iron in multiple sclerosis: a combined imaging and histopathological study at 7 Tesla. Brain. 2011 Dec;134(12):3602–3615.
  • Absinta M, Sati P, Schindler M, et al. Persistent 7-tesla phase rim predicts poor outcome in new multiple sclerosis patient lesions. J Clin Invest. 2016 Jul 1;126(7):2597–2609.
  • Dal-Bianco A, Grabner G, Kronnerwetter C, et al. Slow expansion of multiple sclerosis iron rim lesions: pathology and 7 T magnetic resonance imaging. Acta Neuropathol. 2017 Jan;133(1):25–42.
  • Kaunzner UW, Kang Y, Zhang S, et al. Quantitative susceptibility mapping identifies inflammation in a subset of chronic multiple sclerosis lesions. Brain. 2019 Jan 1;142(1):133–145.
  • Absinta M, Sati P, Masuzzo F, et al. Association of chronic active multiple sclerosis lesions with disability in vivo. JAMA Neurol. 2019 Dec 1;76(12):1520.
  • Dal-Bianco A, Grabner G, Kronnerwetter C, et al. Long-term evolution of multiple sclerosis iron rim lesions in 7 T MRI. Brain. 2021 Apr 12;144(3):833–847.
  • Maggi P, Kuhle J, Schadelin S, et al. Chronic white matter inflammation and serum neurofilament levels in multiple sclerosis. Neurology. 2021 Aug 10;97(6):e543–e553.
  • Kolb H, Absinta M, Beck ES, et al. 7T MRI differentiates remyelinated from demyelinated multiple sclerosis lesions. Ann Neurol. 2021 Oct;90(4):612–626.
  • Rahmanzadeh R, Galbusera R, Lu PJ, et al. A new advanced MRI biomarker for remyelinated lesions in multiple sclerosis. Ann Neurol. 2022 Jun 17;92(3):486–502.
  • Gillen KM, Mubarak M, Park C, et al. QSM is an imaging biomarker for chronic glial activation in multiple sclerosis lesions. Ann Clin Transl Neurol. 2021 Apr;8(4):877–886.
  • Dimov AV, Gillen KM, Nguyen TD, et al. Magnetic susceptibility source separation solely from gradient echo data: histological validation. Tomography. 2022 Jun 14;8(3):1544–1551.
  • Elliott C, Belachew S, Wolinsky JS, et al. Chronic white matter lesion activity predicts clinical progression in primary progressive multiple sclerosis. Brain. 2019 Sep 1;142(9):2787–2799.
  • NAIMS cooperative workshop Feb, 2022. NAIMS consensus statement on imaging chronic active lesions. https://www.naimscooperative.org/2022-naims-workshop
  • Mainero C, Benner T, Radding A, et al. In vivo imaging of cortical pathology in multiple sclerosis using ultra-high field MRI. Neurology. 2009 Sep 22;73(12):941–948.
  • Pitt D, Boster A, Pei W, et al. Imaging cortical lesions in multiple sclerosis with ultra-high-field magnetic resonance imaging. Arch Neurol. 2010 Jul;67(7):812–818.
  • Pinto C, Cambron M, Dobai A, et al. Smoldering lesions in MS: if you like it then you should put a rim on it. Neuroradiology. 2022 Apr;64(4):703–714.
  • Harrison DM, Li X, Liu H, et al. Lesion heterogeneity on high-field susceptibility MRI is associated with multiple sclerosis severity. AJNR Am J Neuroradiol. 2016 Aug;37(8):1447–1453.
  • Marcille M, Hurtado Rua S, Tyshkov C, et al. Disease correlates of rim lesions on quantitative susceptibility mapping in multiple sclerosis. Sci Rep. 2022 Mar 15;12(1):4411.
  • Altokhis AI, Hibbert AM, Allen CM, et al. Longitudinal clinical study of patients with iron rim lesions in multiple sclerosis. Mult Scler. 2022 Aug 24:13524585221114750. doi10.1177/13524585221114750.
  • Solomon AJ, Bourdette DN, Cross AH, et al. The contemporary spectrum of multiple sclerosis misdiagnosis: a multicenter study. Neurology. 2016 Sep 27;87(13):1393–1399.
  • Kollia K, Maderwald S, Putzki N, et al. First clinical study on ultra-high-field MR imaging in patients with multiple sclerosis: comparison of 1.5T and 7T. AJNR Am J Neuroradiol. 2009 Apr;30(4):699–702.
  • Grabner G, Dal-Bianco A, Schernthaner M, et al. Analysis of multiple sclerosis lesions using a fusion of 3.0 T FLAIR and 7.0 T SWI phase: FLAIR SWI. J Magn Reson Imaging. 2011 Mar;33(3):543–549.
  • Absinta M, Sati P, Gaitan MI, et al. Seven-tesla phase imaging of acute multiple sclerosis lesions: a new window into the inflammatory process. Ann Neurol. 2013 Nov;74(5):669–678.
  • Sati P, Thomasson DM, Li N, et al. Rapid, high-resolution, whole-brain, susceptibility-based MRI of multiple sclerosis. Mult Scler. 2014 Oct;20(11):1464–1470.
  • Kilsdonk ID, Wattjes MP, Lopez-Soriano A, et al. Improved differentiation between MS and vascular brain lesions using FLAIR* at 7 Tesla. Eur Radiol. 2014 Apr;24(4):841–849.
  • Yao B, Bagnato F, Matsuura E, et al. Chronic multiple sclerosis lesions: characterization with high-field-strength MR imaging. Radiology. 2012 Jan;262(1):206–215.
  • Sinnecker T, Schumacher S, Mueller K, et al. MRI phase changes in multiple sclerosis vs neuromyelitis optica lesions at 7T. Neurol Neuroimmunol Neuroinflamm. 2016 Aug;3(4):e259.
  • Chawla S, Kister I, Wuerfel J, et al. Iron and non-iron-related characteristics of multiple sclerosis and neuromyelitis optica lesions at 7T MRI. AJNR Am J Neuroradiol. 2016 Jul;37(7):1223–1230.
  • Yao Y, Nguyen TD, Pandya S, et al. Combining quantitative susceptibility mapping with automatic zero reference (QSM0) and Myelin water fraction imaging to quantify iron-related myelin damage in chronic active MS lesions. AJNR Am J Neuroradiol. 2018 Feb;39(2):303–310.
  • Clarke MA, Pareto D, Pessini-Ferreira L, et al. Value of 3T susceptibility-weighted imaging in the diagnosis of multiple sclerosis. AJNR Am J Neuroradiol. 2020 May 21;41(6):1001–1008.
  • Blindenbacher N, Brunner E, Asseyer S, et al. Evaluation of the ‘ring sign’ and the ‘core sign’ as a magnetic resonance imaging marker of disease activity and progression in clinically isolated syndrome and early multiple sclerosis. Mult Scler J Exp Transl Clin. 2020 Jan-Mar;6(1):2055217320915480.
  • Tolaymat B, Zheng W, Chen H, et al. Sex-specific differences in rim appearance of multiple sclerosis lesions on quantitative susceptibility mapping. Mult Scler Relat Disord. 2020;45:102317.
  • Suthiphosuwan S, Sati P, Absinta M, et al. Paramagnetic rim sign in radiologically isolated syndrome. JAMA Neurol. 2020 May 1;77(5):653–655.
  • Maggi P, Sati P, Nair G, et al. Paramagnetic rim lesions are specific to multiple sclerosis: an international multicenter 3T MRI study. Ann Neurol. 2020 Nov;88(5):1034–1042.
  • Maggi P, Absinta M, Sati P, et al. The “central vein sign” in patients with diagnostic “red flags” for multiple sclerosis: a prospective multicenter 3T study. Mult Scler. 2020 Apr;26(4):421–432.
  • Treaba CA, Conti A, Klawiter EC, et al. Cortical and phase rim lesions on 7 T MRI as markers of multiple sclerosis disease progression. Brain Commun. 2021;3(3):fcab134.
  • Tozlu C, Jamison K, Gauthier SA, et al. Dynamic functional connectivity better predicts disability than structural and static functional connectivity in people with multiple sclerosis. Front Neurosci. 2021;15:763966.
  • Micheletti L, Maldonado FR, Watal P, et al. Utility of paramagnetic rim lesions on 1.5-T susceptibility phase imaging for the diagnosis of pediatric multiple sclerosis. Pediatr Radiol. 2022 Jan;52(1):97–103.
  • Comabella M, Clarke MA, Schaedelin S, et al. CSF chitinase 3-like 1 is associated with iron rims in patients with a first demyelinating event. Mult Scler. 2022 Jan;28(1):71–81.
  • Weber CE, Kramer J, Wittayer M, et al. Association of iron rim lesions with brain and cervical cord volume in relapsing multiple sclerosis. Eur Radiol. 2022 Mar;32(3):2012–2022.
  • Hemond CC, Reich DS, Dundamadappa SK. Paramagnetic Rim lesions in multiple sclerosis: comparison of visualization at 1.5-T and 3-T MRI. AJR Am J Roentgenol. 2022 Jul;219(1):120–131.
  • Huang W, Sweeney EM, Kaunzner UW, et al. Quantitative susceptibility mapping versus phase imaging to identify multiple sclerosis iron rim lesions with demyelination. J Neuroimaging. 2022 Jul;32(4):667–675.
  • Kee Kwong KC N, Mollison D, Meijboom R, et al. Rim lesions are demonstrated in early relapsing-remitting multiple sclerosis using 3 T-based susceptibility-weighted imaging in a multi-institutional setting. Neuroradiology. 2022 Jan;64(1):109–117.
  • Krajnc N, Bsteh G, Kasprian G, et al. Peripheral hemolysis in relation to iron rim presence and brain volume in multiple sclerosis. Front Neurol. 2022;13:928582.
  • Oh J, Suthiphosuwan S, Sati P, et al. Cognitive impairment, the central vein sign, and paramagnetic rim lesions in RIS. Mult Scler. 2021 Dec;27(14):2199–2208.
  • Kee Kwong KC N, Mollison D, Meijboom R, et al. The prevalence of paramagnetic rim lesions in multiple sclerosis: a systematic review and meta-analysis. PLoS One. 2021;16(9):e0256845.
  • Clarke M, Cheek R, Clarke R, et al. Paramagnetic rims in treatment naïve persons around the time of multiple sclerosis diagnosis. AAN2022 meeting proceedings, Boston, US. 2022;98.
  • Absinta M, Maric D, Gharagozloo M, et al. A lymphocyte-microglia-astrocyte axis in chronic active multiple sclerosis. Nature. 2021 Sep;597(7878):709–714.
  • Manning A, Clark K, Bar-Or A, et al. Early prediction of CAL evolution from newly developing MS lesions using 7T MRI ACTRIMS Forum 2022 [cited 2022 Feb 25]. https://www.abstractsonline.com/pp8/#!/10495/presentation/309
  • Klistorner S, Barnett MH, Yiannikas C, et al. Expansion of chronic MS lesions is associated with an increase of radial diffusivity in periplaque white matter. Mult Scler. 2022 Apr;28(5):697–706.
  • Thompson AJ, Banwell BL, Barkhof F, et al. Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol. 2018 Feb;17(2):162–173.
  • Filippi M, Preziosa P, Meani A, et al. Performance of the 2017 and 2010 revised McDonald criteria in predicting MS diagnosis after a clinically isolated syndrome: a MAGNIMS study. Neurology. 2022 Jan 4;98(1):e1–e14.
  • Filippi M, Preziosa P, Banwell BL, et al. Assessment of lesions on magnetic resonance imaging in multiple sclerosis: practical guidelines. Brain. 2019 Jul 1;142(7):1858–1875.
  • Wuerfel J, Sinnecker T, Ringelstein EB, et al. Lesion morphology at 7 Tesla MRI differentiates Susac syndrome from multiple sclerosis. Mult Scler. 2012 Nov;18(11):1592–1599.
  • Hagemeier J, Heininen-Brown M, Poloni GU, et al. Iron deposition in multiple sclerosis lesions measured by susceptibility-weighted imaging filtered phase: a case control study. J Magn Reson Imaging. 2012 Jul;36(1):73–83.
  • Hosseini Z, Matusinec J, Rudko DA, et al. Morphology-specific discrimination between MS white matter lesions and benign white matter hyperintensities using ultra-high-field MRI. AJNR Am J Neuroradiol. 2018 Aug;39(8):1473–1479.
  • Jang J, Nam Y, Choi Y, et al. Paramagnetic rims in multiple sclerosis and neuromyelitis optica spectrum disorder: a quantitative susceptibility mapping study with 3-T MRI. J Clin Neurol. 2020 Oct;16(4):562–572.
  • Meaton I, Altokhis A, Allen CM, et al. Paramagnetic rims are a promising diagnostic imaging biomarker in multiple sclerosis. Mult Scler. 2022 Aug 26;Online ahead of print:13524585221118677.
  • Renner B, Verter E, Absinta M, et al. Diagnostic potential of paramagnetic rim lesions for MS in a multicenter setting. Abstract presented at ACTRIMS Forum 2022. 2022.
  • Solomon AJ, Corboy JR. The tension between early diagnosis and misdiagnosis of multiple sclerosis. Nat Rev Neurol. 2017 Sep;13(9):567–572.
  • Geraldes R, Ciccarelli O, Barkhof F, et al. The current role of MRI in differentiating multiple sclerosis from its imaging mimics. Nat Rev Neurol. 2018 Mar 20;14(4):213.
  • Wingerchuk DM, Banwell B, Bennett JL, et al. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology. 2015 Jul 14;85(2):177–189.
  • Kleffner I, Dorr J, Ringelstein M, et al. Diagnostic criteria for Susac syndrome. J Neurol Neurosurg Psychiatry. 2016 Dec;87(12):1287–1295.
  • Absinta M, Cortese IC, Vuolo L, et al. Leptomeningeal gadolinium enhancement across the spectrum of chronic neuroinflammatory diseases. Neurology. 2017 Apr 11;88(15):1439–1444.
  • Absinta M, Sati P, Reich DS. Advanced MRI and staging of multiple sclerosis lesions. Nat Rev Neurol. 2016 Jun;12(6):358–368.
  • Absinta M, Nair G, Monaco MCG, et al. The “central vein sign” in inflammatory demyelination: the role of fibrillar collagen type I. Ann Neurol. 2019 Jun;85(6):934–942.
  • Maggi P, Absinta M, Grammatico M, et al. Central vein sign differentiates multiple sclerosis from central nervous system inflammatory vasculopathies. Ann Neurol. 2018 Feb;83(2):283–294.
  • Sinnecker T, Clarke MA, Meier D, et al. Evaluation of the central vein sign as a diagnostic imaging biomarker in multiple sclerosis. JAMA Neurol. 2019 Aug 19;76(12):1446.
  • Mistry N, Abdel-Fahim R, Samaraweera A, et al. Imaging central veins in brain lesions with 3-T T2*-weighted magnetic resonance imaging differentiates multiple sclerosis from microangiopathic brain lesions. Mult Scler. 2016 Sep;22(10):1289–1296.
  • Solomon AJ, Watts R, Ontaneda D, et al. Diagnostic performance of central vein sign for multiple sclerosis with a simplified three-lesion algorithm. Mult Scler. 2018 May;24(6):750–757.
  • Maggi P, Fartaria MJ, Jorge J, et al. CVSnet: a machine learning approach for automated central vein sign assessment in multiple sclerosis. NMR Biomed. 2020 May;33(5):e4283.
  • Dworkin JD, Sati P, Solomon A, et al. Automated integration of multimodal MRI for the probabilistic detection of the central vein sign in white matter lesions. AJNR Am J Neuroradiol. 2018 Oct;39(10):1806–1813.
  • Ontaneda D, Sati P, Raza P, et al. Central vein sign: a diagnostic biomarker in multiple sclerosis (CAVS-MS) study protocol for a prospective multicenter trial. Neuroimage Clin. 2021;32:102834.
  • Lim T, Suthiphosuwan S, Espiritu A, et al. Paramagnetic rim lesions are predictive of conversion to multiple sclerosis in people with radiologically isolated syndrome: preliminary results from a prospective cohort study. ECTRIMS meeting, Amsterdam. 2022.
  • Zinger N, Ponath G, Sweeney E, et al. Dimethyl fumarate reduces inflammation in chronic active multiple sclerosis lesions. Neurol Neuroimmunol Neuroinflamm. 2022 Mar;9(2):e1138.
  • Eisele P, Wittayer M, Weber CE, et al. Impact of disease-modifying therapies on evolving tissue damage in iron rim multiple sclerosis lesions. Mult Scler. 2022;1:13524585221106338.
  • Hammond KE, Metcalf M, Carvajal L, et al. Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron. Ann Neurol. 2008 Dec;64(6):707–713.
  • Absinta M, Sati P, Fechner A, et al. Identification of chronic active multiple sclerosis lesions on 3T MRI. AJNR Am J Neuroradiol. 2018 Jul;39(7):1233–1238.
  • Barquero G, La Rosa F, Kebiri H, et al. RimNet: a deep 3D multimodal MRI architecture for paramagnetic rim lesion assessment in multiple sclerosis. Neuroimage Clin. 2020;28:102412.
  • Lou C, Sati P, Absinta M, et al. Fully automated detection of paramagnetic rims in multiple sclerosis lesions on 3T susceptibility-based MR imaging. Neuroimage Clin. 2021 Aug 27;32:102796.
  • Zhang H, Nguyen TD, Zhang J, et al. QSMRim-Net: imbalance-aware learning for identification of chronic active multiple sclerosis lesions on quantitative susceptibility maps. Neuroimage Clin. 2022;34:102979.