Magnetresonanztomografie bei Patienten mit Multipler Sklerose: Relevanz in der Diagnose und Verlaufsbeurteilung

Zusammenfassung

Multiple Sklerose (MS) ist eine entzündliche Erkrankung des zentralen Nervensystems, die einen axonal-destruktiven Anteil aufweist, der maßgeblich die Behinderung im Laufe der Erkrankung bestimmt. In den letzten 3 Dekaden etablierte sich die Magnetresonanztomografie (MRT) zum wichtigsten Verfahren in der Diagnosestellung der MS. Die hohe Sensitivität der konventionellen MRT erlaubt die In-vivo-Detektion von fokalen und diffusen entzündlichen Komponenten dieser Erkrankung. Der Nachweis und die Quantifizierung von fokalen Pathologien der in der klinischen Routine eingesetzten MRT trägt entscheidend zur frühen Diagnose der MS bei. Der Nachweis einer Läsionslast im MRT zu Beginn der Erkrankung erhöht die Wahrscheinlichkeit einer frühen Konversion zur klinisch definitiven MS und einer höheren Behinderung in den ersten Jahren der Erkrankung. Dieser diagnostische und prognostische Informationsgewinn zu einem frühen Zeitpunkt der Erkrankung führte 2001 zu einer grundlegenden Revision der diagnostischen Kriterien. Das Konzept der Diagnosestellung beinhaltet klinische und kernspintomografische Kriterien. Diese zuletzt 2010 revidierten diagnostischen Kriterien weisen das Hauptmerkmal auf, dass eine subklinische kernspintomografische Aktivität der Erkrankung einen Schub ersetzt. Darüber hinaus kann die Diagnose MS bereits nach dem ersten Schub und einem MRT gestellt werden, vorausgesetzt es lassen sich kernspintomografische Aktivitätszeichen nachweisen. Die frühe Diagnosestellung unter Berücksichtigung der MRT eröffnet die Möglichkeit einer frühzeitigen Behandlung innerhalb eines offenbar günstigeren therapeutischen Fensters.

Abstract

Multiple sclerosis (MS) is an inflammatory disease of the central nervous system (CNS) with a substantial destructive axonal component that is responsible for the permanent disability accumulating during the course of the disease. Magnetic resonance imaging (MRI) has become the most important method in the diagnosis of MS. The high sensitivity of the MRI permits to detect focal and diffuse inflammatory disease involvement in vivo. In clinical routine the detection and quantification of focal pathology contributes substantially to an early diagnosis of MS. The detection of a substantial lesion load at the beginning of the disease increases the probability of an early conversion to clinically definite MS and the risk of accumulating disability in the first years of the disease. In 2001 this diagnostic and prognostic gain of information at an early stage of the disease resulted in a conceptual shift regarding diagnostic criteria. This concept comprises clinical and MRI criteria. The current 2010 revised criteria follow the concept of substituting a clinical relapse by subclinical MRI activity and allow the diagnosis of MS from one single MRI after the first relapse. This diagnostic approach using MRI allows an early treatment within an appropriate window of treatment opportunity.

^* Beide Autoren haben gleichwertig zum Manuskript beigetragen. Die Reihenfolge ist alphabetisch.

• Literatur

• 1 McDonald WI, Compston A et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 2001; 50: 121-127
• 2 Polman CH, Reingold SC et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Annals of neurology 2011; 69: 292-302
• 3 Wiendl H, Toyka KV et al. Basic and escalating immunomodulatory treatments in multiple sclerosis: current therapeutic recommendations. Journal of neurology 2008; 255: 1449-1463
• 4 Vigeveno RM, Wiebenga OT et al. Shifting imaging targets in multiple sclerosis: from inflammation to neurodegeneration. JMRI 2012; 36: 1-19
• 5 Gass A, Filippi M et al. The contribution of MRI in the differential diagnosis of posterior fossa damage. J Neurol Sci 2000; 172 (Suppl. 01) S43-49
• 6 Miller DH, Filippi M et al. Role of magnetic resonance imaging within diagnostic criteria for multiple sclerosis. Annals of neurology 2004; 56: 273-278
• 7 Palmer S, Bradley WG et al. Subcallosal striations: early findings of multiple sclerosis on sagittal, thin-section, fast FLAIR MR images. Radiology 1999; 210: 149-153
• 8 Fazekas F, Barkhof F et al. The contribution of magnetic resonance imaging to the diagnosis of multiple sclerosis. Neurology 1999; 53: 448-456
• 9 Weier K, Mazraeh J et al. Biplanar MRI for the assessment of the spinal cord in multiple sclerosis. Multiple sclerosis 2012; 18: 1560-1569
• 10 Lycklama G, Thompson A et al. Spinal-cord MRI in multiple sclerosis. Lancet Neurol 2003; 2: 555-562
• 11 Bot JC, Barkhof F et al. Spinal cord abnormalities in recently diagnosed MS patients: added value of spinal MRI examination. Neurology 2004; 62: 226-233
• 12 Coret F, Bosca I et al. Early diffuse demyelinating lesion in the cervical spinal cord predicts a worse prognosis in relapsing-remitting multiple sclerosis. Multiple sclerosis 2010; 16: 935-941
• 13 Lavdas E, Mavroidis P et al. Reduction of motion, truncation and flow artifacts using BLADE sequences in cervical spine MR imaging. Magnetic resonance imaging 2015; 33: 194-200
• 14 Sombekke MH, Wattjes MP et al. Spinal cord lesions in patients with clinically isolated syndrome: a powerful tool in diagnosis and prognosis. Neurology 2013; 80: 69-75
• 15 O’Riordan JI, Losseff NA et al. Asymptomatic spinal cord lesions in clinically isolated optic nerve, brain stem, and spinal cord syndromes suggestive of demyelination. J Neurol Neurosurg Psychiatry 1998; 64: 353-357
• 16 Brex PA, O’Riordan JI et al. Multisequence MRI in clinically isolated syndromes and the early development of MS. Neurology 1999; 53: 1184-1190
• 17 Okuda DT, Mowry EM et al. Incidental MRI anomalies suggestive of multiple sclerosis: the radiologically isolated syndrome. Neurology 2009; 72: 800-805
• 18 Okuda DT, Mowry EM et al. Asymptomatic spinal cord lesions predict disease progression in radiologically isolated syndrome. Neurology 2011; 76: 686-692
• 19 Bot JC, Barkhof F et al. Differentiation of multiple sclerosis from other inflammatory disorders and cerebrovascular disease: value of spinal MR imaging. Radiology 2002; 223: 46-56
• 20 Schumacker GA, Beebe G et al. Problems of Experimental Trials of Therapy in Multiple Sclerosis: Report by the Panel on the Evaluation of Experimental Trials of Therapy in Multiple Sclerosis. Annals of the New York Academy of Sciences 1965; 122: 552-568
• 21 Barkhof F, Filippi M et al. Comparison of MRI criteria at first presentation to predict conversion to clinically definite multiple sclerosis. Brain 1997; 120: 2059-2069
• 22 Tintore M, Rovira A et al. New diagnostic criteria for multiple sclerosis: application in first demyelinating episode. Neurology 2003; 60: 27-30
• 23 Swanton JK, Rovira A et al. MRI criteria for multiple sclerosis in patients presenting with clinically isolated syndromes: a multicentre retrospective study. Lancet neurology 2007; 6: 677-686
• 24 Montalban X, Tintore M et al. MRI criteria for MS in patients with clinically isolated syndromes. Neurology 2010; 74: 427-434
• 25 Barkhof F, Filippi M et al. Improving interobserver variation in reporting gadolinium-enhanced MRI lesions in multiple sclerosis. Neurology 1997; 49: 1682-1688
• 26 Molyneux PD, Miller DH et al. Visual analysis of serial T2-weighted MRI in multiple sclerosis: intra- and interobserver reproducibility. Neuroradiology 1999; 41: 882-888
• 27 van Walderveen MA, Truyen L et al. Development of hypointense lesions on T1-weighted spin-echo magnetic resonance images in multiple sclerosis: relation to inflammatory activity. Arch Neurol 1999; 56: 345-351
• 28 Gass A, Radu EW et al. [MRI follow-up in multiple sclerosis. A guideline for quality assurance]. Rofo 1999; 170: 581-586
• 29 Filippi M, Rocca MA et al. EFNS guidelines on the use of neuroimaging in the management of multiple sclerosis. Eur J Neurol 2006; 13: 313-325
• 30 Simon JH, Li D et al. Standardized MR imaging protocol for multiple sclerosis: Consortium of MS Centers consensus guidelines. Am J Neuroradiol 2006; 27: 455-461
• 31 Sailer M, Fischl B et al. Focal thinning of the cerebral cortex in multiple sclerosis. Brain 2003; 126: 1734-1744
• 32 Korteweg T, Tintore M et al. MRI criteria for dissemination in space in patients with clinically isolated syndromes: a multicentre follow-up study. Lancet Neurol 2006; 5: 221-227
• 33 Sailer M, Fazekas F et al. [Cerebral and spinal MRI examination in patients with clinically isolated syndrome and definite multiple sclerosis]. Rofo 2008; 180: 994-1001
• 34 Dalton CM, Brex PA et al. New T2 lesions enable an earlier diagnosis of multiple sclerosis in clinically isolated syndromes. Annals of neurology 2003; 53: 673-676
• 35 Weiner HL, Guttmann CR et al. Serial magnetic resonance imaging in multiple sclerosis: correlation with attacks, disability, and disease stage. J Neuroimmunol 2000; 104: 164-173
• 36 Brex PA, Ciccarelli O et al. A longitudinal study of abnormalities on MRI and disability from multiple sclerosis. N Engl J Med 2002; 346: 158-164
• 37 Sormani MP, Bruzzi P et al. MRI metrics as surrogate markers for clinical relapse rate in relapsing-remitting MS patients. Neurology 2002; 58: 417-421
• 38 Sormani MP, Bonzano L et al. Surrogate endpoints for EDSS worsening in multiple sclerosis. A meta-analytic approach. Neurology 2010; 75: 302-309
• 39 Sormani MP, Stubinski B et al. Magnetic resonance active lesions as individual-level surrogate for relapses in multiple sclerosis. Mult Scler 2011; 17: 541-549
• 40 Sormani MP, Arnold DL et al. Treatment effect on brain atrophy correlates with treatment effect on disability in multiple sclerosis. Annals of neurology 2014; 75: 43-49
• 41 Freedman MS, Patry DG et al. Treatment optimization in multiple sclerosis. Can J Neurol Sci 2004; 31: 157-168
• 42 Rio J, Comabella M et al. Multiple sclerosis: current treatment algorithms. Curr Opin Neurol 2011; 24: 230-237
• 43 Sormani M, Rio J et al. Scoring treatment response in patients with relapsing multiple sclerosis. Mult Scler 2013; 19: 605-612
• 44 Stangel M, Penner IK et al. Multiple Sclerosis Decision Model (MSDM): Entwicklung eines Mehrfaktorenmodells zur Beurteilung des Therapie- und Krankheitsverlaufs bei schubförmiger Multipler Sklerose. Akt Neurol 2013; 40: 486-493
• 45 Wattjes MP, Barkhof F. Diagnosis of natalizumab-associated progressive multifocal leukoencephalopathy using MRI. Current Opinion in Neurology 2014; 27: 260-270
• 46 Warnke C, Menge T et al. Natalizumab and progressive multifocal leukoencephalopathy: what are the causal factors and can it be avoided?. Archives of Neurology 2010; 67: 923-930
• 47 Bloomgren G, Richman S et al. Risk of natalizumab-associated progressive multifocal leukoencephalopathy. The New England journal of medicine 2012; 366: 1870-1880
• 48 Yousry TA, Pelletier D et al. Magnetic resonance imaging pattern in natalizumab-associated progressive multifocal leukoencephalopathy. Annals of neurology 2012; 72: 779-787
• 49 Wattjes MP, Richert ND et al. The chameleon of neuroinflammation: magnetic resonance imaging characteristics of natalizumab-associated progressive multifocal leukoencephalopathy. Multiple Sclerosis 2013; 19: 1826-1840
• 50 Tas MW, Barkhol F et al. The effect of gadolinium on the sensitivity and specificity of MR in the initial diagnosis of multiple sclerosis. Am J Neuroradiol 1995; 16: 259-264
• 51 Kappos L, Moeri D et al. Predictive value of gadolinium-enhanced magnetic resonance imaging for relapse rate and changes in disability or impairment in multiple sclerosis: a meta-analysis. Gadolinium MRI Meta-analysis Group. Lancet 1999; 353: 964-969
• 52 Filippi M, Yousry T et al. Comparison of triple dose versus standard dose gadolinium-DTPA for detection of MRI enhancing lesions in patients with MS. Neurology 1996; 46: 379-384
• 53 Fazekas F, Soelberg-Sorensen P et al. MRI to monitor treatment efficacy in multiple sclerosis. Journal of neuroimaging 2007; 17 (Suppl. 01) 50S-55S
• 54 Kanda T, Fukusato T, Matsuda M et al. Gadolinium-based Contrast Agent Accumulates in the Brain Even in Subjects without Severe Renal Dysfunction: Evaluation of Autopsy Brain Specimens with Inductively Coupled Plasma Mass Spectroscopy. Radiology 2015; 276: 228-232
• 55 Stojanov DA, Aracki-Trenkic A, Vojinovic S et al. Increasing signal intensity within the dentate nucleus and globus pallidus on unenhanced T1W magnetic resonance images in patients with relapsing-remitting multiple sclerosis: correlation with cumulative dose of a macrocyclic gadolinium-based contrast agent, gadobutrol. Eur Radiol 2015; DOI: 10.1007/s00330-015-3879-9.
• 56 Filippi M, van Waesberghe JH et al. Interscanner variation in brain MRI lesion load measurements in MS: implications for clinical trials. Neurology 1997; 49: 371-377
• 57 Schima W, Wimberger D et al. [The importance of magnetic field strength in the MR diagnosis of multiple sclerosis: a comparison of 0.5 and 1.5 T]. RoFo 1993; 158: 368-371
• 58 Lee DH, Vellet AD et al. MR imaging field strength: prospective evaluation of the diagnostic accuracy of MR for diagnosis of multiple sclerosis at 0.5 and 1.5 T. Radiology 1995; 194: 257-262
• 59 Sicotte NL, Voskuhl RR et al. Comparison of multiple sclerosis lesions at 1.5 and 3.0 Tesla. Invest Radiol 2003; 38: 423-427
• 60 Bachmann R, Reilmann R et al. FLAIR imaging for multiple sclerosis: a comparative MR study at 1.5 and 3.0 Tesla. European radiology 2006; 16: 915-921
• 61 Wattjes MP, Lutterbey GG et al. Higher sensitivity in the detection of inflammatory brain lesions in patients with clinically isolated syndromes suggestive of multiple sclerosis using high field MRI: an intraindividual comparison of 1.5 T with 3.0 T. Eur Radiol 2006; 16: 2067-2073
• 62 Barkhof F, Pouwels PJ et al. The Holy Grail in diagnostic neuroradiology: 3T or 3D?. European radiology 2011; 21: 449-456
• 63 Tan IL, Pouwels PJ et al. Isotropic 3D fast FLAIR imaging of the brain in multiple sclerosis patients: initial experience. Eur Radiol 2002; 12: 559-567
• 64 Patzig M, Burke M et al. Comparison of 3D cube FLAIR with 2D FLAIR for multiple sclerosis imaging at 3 Tesla. RoFo 2014; 186: 484-488
• 65 Gramsch C, Nensa F et al. Diagnostic value of 3D fluid attenuated inversion recovery sequence in multiple sclerosis. Acta radiologica 2015; 56: 622-627
• 66 Vrenken H, Jenkinson M et al. Recommendations to improve imaging and analysis of brain lesion load and atrophy in longitudinal studies of multiple sclerosis. Journal of neurology 2012; 260: 2458-2471
• 67 Bevan CJ, Cree BA. Disease activity free status: a new end point for a new era in multiple sclerosis clinical research?. JAMA Neurology 2014; 71: 269-270
• 68 Rotstein DL, Healy BC et al. Evaluation of no evidence of disease activity in a 7-year longitudinal multiple sclerosis cohort. JAMA Neurology 2015; 72: 152-158
• 69 Calabrese M, Rocca MA et al. A 3-year magnetic resonance imaging study of cortical lesions in relapse-onset multiple sclerosis. Ann Neurol 2010; 67: 376-383
• 70 Geurts JJ, Calabrese M et al. Measurement and clinical effect of grey matter pathology in multiple sclerosis. Lancet Neurology 2012; 11: 1082-1092
• 71 Fisher E, Lee JC et al. Gray matter atrophy in multiple sclerosis: a longitudinal study. Annals of neurology 2008; 64: 255-265
• 72 Fisniku LK, Chard DT et al. Gray matter atrophy is related to long-term disability in multiple sclerosis. Annals of Neurology 2008; 64: 247-254
• 73 Redpath TW, Smith FW. Technical note: use of a double inversion recovery pulse sequence to image selectively grey or white brain matter. Br J Radiol 1994; 67: 1258-1263
• 74 Geurts JJ, Bo L et al. Cortical lesions in multiple sclerosis: combined postmortem MR imaging and histopathology. Am J Neuroradiol 2005; 26: 572-577
• 75 Seewann A, Kooi EJ et al. Postmortem verification of MS cortical lesion detection with 3D DIR. Neurology 2012; 78: 302-308
• 76 Calabrese M, Agosta F et al. Cortical lesions and atrophy associated with cognitive impairment in relapsing-remitting multiple sclerosis. Arch Neurol 2009; 66: 1144-1150
• 77 Calabrese M, Filippi M et al. Cortical lesions in multiple sclerosis. Nat Rev Neurol 2010; 6: 438-444
• 78 Calabrese M, Romualdi C et al. The changing clinical course of multiple sclerosis: A matter of grey matter. Ann Neurol 2013; 74: 76-83
• 79 Filippi M, Rocca MA et al. Intracortical lesions: relevance for new MRI diagnostic criteria for multiple sclerosis. Neurology 2010; 75: 1988-1994
• 80 Geurts JJ, Roosendaal SD et al. Consensus recommendations for MS cortical lesion scoring using double inversion recovery MRI. Neurology 2011; 76: 418-424
• 81 Absinta M, Rocca MA et al. Patients with migraine do not have MRI-visible cortical lesions. Journal of neurology 2012; 259: 2695-2698
• 82 Calabrese M, Oh MS et al. No MRI evidence of cortical lesions in neuromyelitis optica. Neurology 2012; 79: 1671-1676
• 83 Kremenchutzky M. Venocentric lesions: an MRI marker of MS?. Front Neurol 2013; 4: 98
• 84 Tan IL, van Schijndel RA et al. MR venography of multiple sclerosis. Am J Neuroradiol 2000; 21: 1039-1042
• 85 Tallantyre EC, Morgan PS et al. A comparison of 3T and 7T in the detection of small parenchymal veins within MS lesions. Investigative radiology 2009; 44: 491-494
• 86 Mistry N, Dixon J et al. Central Veins in Brain Lesions Visualized With High-Field Magnetic Resonance Imaging. JAMA Neurology 2013; 70: 623
• 87 Tallantyre EC, Dixon JE et al. Ultra-high-field imaging distinguishes MS lesions from asymptomatic white matter lesions. Neurology 2011; 76: 534-539
• 88 Sinnecker T, Dorr J et al. Distinct lesion morphology at 7-T MRI differentiates neuromyelitis optica from multiple sclerosis. Neurology 2012; 79: 708-714
• 89 Wuerfel J, Sinnecker T et al. Lesion morphology at 7 Tesla MRI differentiates Susac syndrome from multiple sclerosis. Multiple sclerosis 2012; 18: 1592-1599
• 90 Lummel N, Boeckh-Behrens T et al. Presence of a central vein within white matter lesions on susceptibility weighted imaging: a specific finding for multiple sclerosis?. Neuroradiology 2011; 53: 311-317