Longitudinal analysis of new multiple sclerosis lesions with magnetization transfer and diffusion tensor imaging

. 2024 Mar ; 34 (3) : 1680-1691. [epub] 20230902

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37658894

Grantová podpora
Swiss Multiple Sclerosis Society Swiss Multiple Sclerosis Society

Odkazy

PubMed 37658894
PubMed Central PMC10873225
DOI 10.1007/s00330-023-10173-6
PII: 10.1007/s00330-023-10173-6
Knihovny.cz E-zdroje

OBJECTIVE: The potential of magnetization transfer imaging (MTI) and diffusion tensor imaging (DTI) for the detection and evolution of new multiple sclerosis (MS) lesions was analyzed. METHODS: Nineteen patients with MS obtained conventional MRI, MTI, and DTI examinations bimonthly for 12 months and again after 24 months at 1.5 T MRI. MTI was acquired with balanced steady-state free precession (bSSFP) in 10 min (1.3 mm3 isotropic resolution) yielding both magnetization transfer ratio (MTR) and quantitative magnetization transfer (qMT) parameters (pool size ratio (F), exchange rate (kf), and relaxation times (T1/T2)). DTI provided fractional anisotropy (FA), mean diffusivity (MD), axial diffusivity (AD), and radial diffusivity (RD). RESULTS: At the time of their appearance on MRI, the 21 newly detected MS lesions showed significantly reduced MTR/F/kf and prolonged T1/T2 parameters, as well as significantly reduced FA and increased AD/MD/RD. Significant differences were already observed for MTR 4 months and for qMT parameters 2 months prior to lesions' detection on MRI. DTI did not show any significant pre-lesional differences. Slightly reversed trends were observed for most lesions up to 8 months after their detection for qMT and less pronounced for MTR and three diffusion parameters, while appearing unchanged on MRI. CONCLUSIONS: MTI provides more information than DTI in MS lesions and detects tissue changes 2 to 4 months prior to their appearance on MRI. After lesions' detection, qMT parameter changes promise to be more sensitive than MTR for the lesions' evolutional assessment. Overall, bSSFP-based MTI adumbrates to be more sensitive than MRI and DTI for the early detection and follow-up assessment of MS lesions. CLINICAL RELEVANCE STATEMENT: When additionally acquired in routine MRI, fast bSSFP-based MTI can complement the MRI/DTI longitudinal lesion assessment by detecting MS lesions 2-4 months earlier than with MRI, which could implicate earlier clinical decisions and better follow-up/treatment assessment in MS patients. KEY POINTS: • Magnetization transfer imaging provides more information than DTI in multiple sclerosis lesions and can detect tissue changes 2 to 4 months prior to their appearance on MRI. • After lesions' detection, quantitative magnetization transfer changes are more pronounced than magnetization transfer ratio changes and therefore promise to be more sensitive for the lesions' evolutional assessment. • Balanced steady-state free precession-based magnetization transfer imaging is more sensitive than MRI and DTI for the early detection and follow-up assessment of multiple sclerosis lesions.

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Inglese M, Grossman RI, Filippi M. Magnetic resonance imaging monitoring of multiple sclerosis lesion evolution. J Neuroimaging. 2005;15(4 Suppl):22S–29S. PubMed

Granziera C, Wuerfel J, Barkhof F et al (2021) Quantitative magnetic resonance imaging towards clinical application in multiple sclerosis. Brain 144:1296–1311 PubMed PMC

Li L, Chopp M, Nejad-Davarani SP et al (2014) Perfusion and diffusion abnormalities of multiple sclerosis lesions and relevance of classified lesions to disease status. J Neurol Neurophysiol 2014:12. 10.4172/2155-9562.S12-012 PubMed PMC

Liu Y, Mitchell PJ, Kilpatrick TJ et al (2012) Diffusion tensor imaging of acute inflammatory lesion evolution in multiple sclerosis. J Clin Neurosci 19:1689–1694 PubMed

Ontaneda D, Sakaie K, Lin J et al (2014) Identifying the start of multiple sclerosis injury: a serial DTI study. J Neuroimaging 24:569–576 PubMed PMC

Levesque IR, Giacomini PS, Narayanan S, Ribeiro LT, Sled JG, Arnold DL, et al. Quantitative magnetization transfer and myelin water imaging of the evolution of acute multiple sclerosis lesions. Magn Reson Med. 2010;63:633–640. doi: 10.1002/mrm.22244. PubMed DOI

O’Muircheartaigh J, Vavasour I, Ljungberg E et al (2019) Quantitative neuroimaging of myelin in the healthy brain and in multiple sclerosis. Hum Brain Mapp 40:2104–2116 PubMed PMC

Lommers E, Simon J, Reuter G et al (2019) Multiparameter MRI quantification of microstructural tissue alterations in multiple sclerosis. Neuroimage Clin 23:101879 PubMed PMC

Dousset V, Gayou A, Brochet B, Caille JM. Early structural changes in acute MS lesions assessed by serial magnetization transfer studies. Neurology. 1998;51:1150–1155. doi: 10.1212/WNL.51.4.1150. PubMed DOI

Filippi M, Rocca MA, Martino G, Horsfield MA, Comi G. Magnetization transfer changes in the normal appearing white matter precede the appearance of enhancing lesions in patients with multiple sclerosis. Ann Neurol. 1998;43:809–814. doi: 10.1002/ana.410430616. PubMed DOI

Pike GB, De Stefano N, Narayanan S et al (2000) Multiple sclerosis: magnetization transfer MR imaging of white matter before lesion appearance on T2-weighted images. Radiology 215:824–830 PubMed

Ropele S, Strasser-Fuchs S, Augustin M et al (2000) A comparison of magnetization transfer ratio, magnetization transfer rate, and the native relaxation time of water protons related to relapsing-remitting multiple sclerosis. AJNR Am J Neuroradiol 21:1885–1891 PubMed PMC

Karampekios S, Papanikolaou N, Papadaki E et al (2005) Quantification of magnetization transfer rate and native T1 relaxation time of the brain: correlation with magnetization transfer ratio measurements in patients with multiple sclerosis. Neuroradiology 47:189–196 PubMed

Rahmanzadeh R, Weigel M, Lu PJ et al (2022) A comparative assessment of myelin-sensitive measures in multiple sclerosis patient and healthy subjects. Neroimage Clin 36:103177 PubMed PMC

Elliott C, Momayyezsiahkal P, Arnold DL et al (2021) Abnormalities in normal-appearing white matter from which multiple sclerosis lesions arise. Brain Commun 10(3):fcab176 PubMed PMC

Gloor M, Scheffler K, Bieri O. Quantitative magnetization transfer imaging using balanced SSFP. Magn Reson Med. 2008;60:691–700. doi: 10.1002/mrm.21705. PubMed DOI

Garcia M, Gloor M, Radue EW et al (2012) Fast high-resolution brain imaging with balanced SSFP: interpretation of quantitative magnetization transfer towards simple MTR. Neuroimage 59:202–211 PubMed

Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208-219 PubMed

Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res Int J. 1996;29:162–173. doi: 10.1006/cbmr.1996.0014. PubMed DOI

Deoni SC, Peters TM, Rutt BK. High-resolution T1 and T2 mapping of the brain in a clinically acceptable time with DESPOT1 and DESPOT2. Magn Reson Med. 2005;53:237–241. doi: 10.1002/mrm.20314. PubMed DOI

Homer J, Roberts JK. Conditions for the driven equilibrium single pulse observation of spin-lattice relaxation times. J Magn Reson. 1969;74:424–432.

Yushkevich PA, Piven J, Hazlett HC et al (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128 PubMed

Rocca MA, Cercignani M, Iannucci G, Comi G, Filippi M. Weekly diffusion-weighted imaging of normal-appearing white matter in MS. Neurology. 2000;55:882–884. doi: 10.1212/WNL.55.6.882. PubMed DOI

Werring DJ, Brassat D, Droogan AG et al (2000) The pathogenesis of lesions and normal-appearing white matter changes in multiple sclerosis: a serial diffusion MRI study. Brain J Neurol 123:1667–1676 PubMed

Narayna PA, Doyle TJ, Lai D, Wolinsky JS. Serial proton magnetic resonance spectroscopic imaging, contrast-enhanced magnetic resonance imaging, and quantitative lesion volumetry in multiple sclerosis. Ann Neurol. 1998;43:56–71. doi: 10.1002/ana.410430112. PubMed DOI

Silver NC, Lai M, Symms MR, Barker GJ, McDonald WI, Miller DH. Serial magnetization transfer imaging to characterize the early evolution of new MS lesions. Neurology. 1998;51:758–764. doi: 10.1212/WNL.51.3.758. PubMed DOI

Goodkin DE, Rooney WD, Sloan R et al (1998) A serial study of new MS lesions and the white matter from which they arise. Neurology 51:1689–1697 PubMed

Fazekas F, Ropele S, Enzinger C, Seifert T, Strasser-Fuchs S. Quantitative magnetization transfer imaging of pre-lesional white-matter changes in multiple sclerosis. Mult Scler. 2002;8:479–484. doi: 10.1191/1352458502ms860oa. PubMed DOI

York EN, Thrippleton MJ, Meijboom R, Hunt DPJ, Waldman AD. Quantitative magnetization transfer imaging in relapsing-remitting multiple sclerosis: a systematic review and meta-analysis. Brain Comm. 2022;4(2):fcac088. doi: 10.1093/braincomms/fcac088. PubMed DOI PMC

Giacomini PS, Levesque I, Ribeiro L et al (2009) Measuring demyelination and remyelination in acute multiple sclerosis lesion voxels. Arch Neurol 66:375–381 PubMed

Moccia M, van de Pavert S, Eshaghi A et al (2020) Pathologic correlates of the magnetization transfer ratio in multiple sclerosis. Neurology 95:e2965–e2976 PubMed

York EN, Meijboom R, Thrippleton MJ et al (2022) Longitudinal microstructural MRI markers of demyelination and neurodegeneration in early relapsing-remitting multiple sclerosis: magnetization transfer, water diffusion and g-ratio. Neuroimage Clin 36:103228 PubMed PMC

Brown RA, Narayanan S, Arnold DL. Imaging of repeated episodes of demyelination and remyelination in multiple sclerosis. NeuroImage Clin. 2014;6:20–25. doi: 10.1016/j.nicl.2014.06.009. PubMed DOI PMC

Yarnykh VL, Bowen JD, Samsonov A et al (2015) Fast whole-brain three-dimensional macromolecular proton fraction mapping in multiple sclerosis. Radiology 274:210–220 PubMed PMC

Garcia M, Gloor M, Bieri O et al (2015) Imaging of primary brain tumors and metastases with fast quantitative 3-dimensional magnetization transfer. J Neuroimaging 25:1007–1014 PubMed

Turati L, Moscatelli M, Mastropietro A et al (2015) In vivo quantitative magnetization transfer imaging correlates with histology during de- and remyelination in cuprizone-treated mice. NMR Biomed 28:327–337 PubMed

Schmierer K, Tozer DJ, Scaravilli F et al (2007) Quantitative magnetization transfer imaging in postmortem multiple sclerosis brain. J Magn Reson Imaging 26:41–51 PubMed PMC

Sled JG. Modelling and interpretation of magnetization transfer imaging in the brain. Neuroimage. 2018;182:128–135. doi: 10.1016/j.neuroimage.2017.11.065. PubMed DOI

Droby A, Fleischer V, Carnini M et al (2015) The impact of isolated lesions on white-matter fiber tracts in multiple sclerosis patients. Neuroimage Clin 8:110–116 PubMed PMC

Klistorner A, Vootakuru N, Wang C et al (2015) Decoding diffusivity in multiple sclerosis: analysis of optic radiation lesional and non-lesional white matter. PLoS One 10:e0122114 PubMed PMC

Monohan E, Vargas WS, Monohan E et al (2015) Measuring longitudinal myelin water fraction in new multiple sclerosis lesions. Neuroimage Clin 9:369–375 PubMed PMC

Kolind S, Seddigh A, Combes A et al (2015) Brain and cord myelin water imaging: a progressive multiple sclerosis biomarker. Neuroimage Clin 9:574–580 PubMed PMC

Commowick O, Fillard P, Clatz O, Warfield SK. Detection of DTI white matter abnormalities in multiple sclerosis patients. Med Image Comput Comput Assist Interv. 2008;11:975–982. PubMed PMC

Kitzler HH, Su J, Zeineh M et al (2012) Deficient MWF mapping in multiple sclerosis using 3D whole-brain multi-component relaxation MRI. Neuroimage 59:2670–2677 PubMed PMC

Zhang Y, Gauthier SA, Gupta A et al (2018) Longitudinal change in magnetic susceptibility of new enhanced multiple sclerosis (MS) lesions measured on serial quantitative susceptibility mapping (QSM). Radiology 289:487–496 PubMed PMC

Wang Y, Sun P, Wang Q et al (2015) Differentiation and quantification of inflammation, demyelination and axon injury or loss in multiple sclerosis. Brain 138:1223–1238 PubMed PMC

Rovira A, Alonso J, Cucurella G et al (1999) Evolution of multiple sclerosis lesions on serial contrast-enhanced T1-weighted and magnetization-transfer MR images. AJNR Am J Neuroradiol 20:1939–1945 PubMed PMC

Tagge IJ, Leppert IR, Fetco D et al (2022) Permanent tissue damage in multiple sclerosis lesions is associated with reduced pre-lesion myelin and axon volume fractions. Mult Scler 28:2027–2037 PubMed PMC

Van Waesberghe JH, van Walderveen MA, Castelijns JA et al (1998) Patterns of lesion development in multiple sclerosis: longitudinal observations with T1-weighted spin-echo and magnetization transfer MR. AJNR Am J Neuroradiol 19:675–683 PubMed PMC

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