Ultrahigh field MRI in clinical neuroimmunology: a potential contribution to improved diagnostics and personalised disease management

EPMA Journal

Jens Wuerfel³  Friedemann Paul⁴  Thoralf Niendorf⁷  Jan Dörr⁶  Petr Dusek¹  Joseph Kuchling⁵  Tim Sinnecker² 

[1]Department of Neurology and Center of Clinical Neuroscience, Charles University in Prague, 1st Faculty of Medicine and General University Hospital in Prague, Kateřinská 30, Praha 2, 128 21, Czech Republic

[2]Department of Neurology, Asklepios Fachklinikum Teupitz, Buchholzer Str. 21, Teupitz, 15755, Germany

[3]Medical Image Analysis Center, Mittlere Strasse 83, Basel, CH-4031, Switzerland

[4]Department of Neurology, Charité - Universitaetsmedizin Berlin, Charitéplatz 1, Berlin, 10117, Germany

[5]NeuroCure Clinical Research Center (NCRC), Charité - Universitaetsmedizin Berlin, Charitéplatz 1, Berlin, 10117, Germany

[6]Clinical and Experimental Multiple Sclerosis Research Center, Department of Neurology, Charité Universitaetsmedizin Berlin, Charitéplatz 1, Berlin, 10117, Germany

[7]Experimental and Clinical Research Center, Charité - Universitaetsmedizin Berlin and Max Delbrueck Center for Molecular Medicine, Robert-Roessle-Strasse 10, Berlin, 13125, Germany

关键词: Predictive, Preventive and Personalised Medicine;    Cortical lesions;    Central vein sign;    Neuroimmunology;    Susac syndrome;    Neuromyelitis optica;    Multiple sclerosis;    Ultrahigh field MRI;    7 Tesla;   

Others  :  1224080
DOI  :  10.1186/s13167-015-0038-y

 received in 2015-07-03, accepted in 2015-07-20,  发布年份 2015

【 摘 要 】

Conventional magnetic resonance imaging (MRI) at 1.5 Tesla (T) is limited by modest spatial resolution and signal-to-noise ratio (SNR), impeding the identification and classification of inflammatory central nervous system changes in current clinical practice. Gaining from enhanced susceptibility effects and improved SNR, ultrahigh field MRI at 7 T depicts inflammatory brain lesions in great detail. This review summarises recent reports on 7 T MRI in neuroinflammatory diseases and addresses the question as to whether ultrahigh field MRI may eventually improve clinical decision-making and personalised disease management.

【 授权许可】

   
2015 Sinnecker et al.

【 图 表 】

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【 参考文献 】

• [1]Holland GN, Moore WS, Hawkes RC. Nuclear magnetic resonance tomography of the brain. J Comput Assist Tomogr. 1980; 4:1-3.
• [2]Filippi M, Rocca MA, De Stefano N, Enzinger C, Fisher E, Horsfield MA et al.. Magnetic resonance techniques in multiple sclerosis: the present and the future. Arch Neurol. 2011; 68:1514-20.
• [3]Kuchling J, Sinnecker T, Bozin I, Dörr J, Madai VI, Sobesky J et al.. Ultrahigh field MRI in context of neurological diseases. Nervenarzt. 2014; 85(4):445-58.
• [4]Golubnitschaja O, Costigliola V. EPMA. General report & recommendations in predictive, preventive and personalised medicine 2012: white paper of the European Association for Predictive, Preventive and Personalised Medicine. EPMA J. 2012; 3:1-53.
• [5]Haacke E, Brown R, Thompson M, Venkatesan R. Magnetic resonance imaging: physical principles and sequence design. John Wiley & Sons (USA). 1999. p. 378.
• [6]Moser E, Stahlberg F, Ladd ME, Trattnig S. 7-T MR—from research to clinical applications? NMR Biomed. 2012; 25:695-716.
• [7]Gizewski ER, Maderwald S, Linn J, Dassinger B, Bochmann K, Forsting M et al.. High-resolution anatomy of the human brain stem using 7-T MRI: improved detection of inner structures and nerves? Neuroradiology. 2014; 56:177-86.
• [8]Strotmann B, Heidemann RM, Anwander A, Weiss M, Trampel R, Villringer A et al.. High-resolution MRI and diffusion-weighted imaging of the human habenula at 7 tesla. J Magn Reson Imaging. 2014; 39:1018-26.
• [9]Graessl A, Renz W, Hezel F, Dieringer MA, Winter L, Oezerdem C et al.. Modular 32-channel transceiver coil array for cardiac MRI at 7.0T: modular transceiver coil array for cardiac MRI. Magn Reson Med. 2014; 72:276-90.
• [10]Graessl A, Muhle M, Schwerter M, Rieger J, Oezerdem C, Santoro D et al.. Ophthalmic magnetic resonance imaging at 7 T using a 6-channel transceiver radiofrequency coil array in healthy subjects and patients with intraocular masses. Invest Radiol. 2014; 49:260-70.
• [11]Thalhammer C, Renz W, Winter L, Hezel F, Rieger J, Pfeiffer H et al.. Two-dimensional sixteen channel transmit/receive coil array for cardiac MRI at 7.0 T: design, evaluation, and application. J Magn Reson Imaging. 2012; 36:847-57.
• [12]Atkinson IC, Renteria L, Burd H, Pliskin NH, Thulborn KR. Safety of human MRI at static fields above the FDA 8 T guideline: sodium imaging at 9.4 T does not affect vital signs or cognitive ability. J Magn Reson Imaging. 2007; 26:1222-7.
• [13]Chakeres DW, Bornstein R, Kangarlu A. Randomized comparison of cognitive function in humans at 0 and 8 Tesla. J Magn Reson Imaging. 2003; 18:342-5.
• [14]Theysohn J. Subjective acceptance of 7T: initial experience in the first 210 subjects. Proc Intl Soc Mag Reson Med. 2008;16:1049.
• [15]Möller HE, von Cramon DY. Survey of risks related to static magnetic fields in ultra high field MRI. Rofo – Fortschr Rontg. 2008; 180:293-301.
• [16]Fatahi M, Reddig A, Friebe B, Reinhold D, Speck O. Analysis of DNA double-strand breaks in human peripheral blood mononuclear cells after exposure to 7T MRI. ISMRM Toronto, Canada. 2015; 2015:0300.
• [17]Klix S, Els A, Paul K, Graessl A, Oezerdem C, Weinberger O et al.. On the subjective acceptance during cardiovascular magnetic resonance imaging at 7.0 Tesla. PLOS ONE. 2015; 10: Article ID e0117095
• [18]Chakeres DW, de Vocht F. Static magnetic field effects on human subjects related to magnetic resonance imaging systems. Prog Biophys Mol Biol. 2005; 87:255-65.
• [19]Kangarlu A, Robitaille P-ML. Biological effects and health implications in magnetic resonance imaging. Concepts Magn Reson. 2000; 12:321-59.
• [20]Lee JW, Kim MS, Kim YJ, Choi YJ, Lee Y, Chung HW. Genotoxic effects of 3 T magnetic resonance imaging in cultured human lymphocytes. Bioelectromagnetics. 2011; 32:535-42.
• [21]Knuuti J, Saraste A, Kallio M, Minn H. Is cardiac magnetic resonance imaging causing DNA damage? Eur Heart J. 2013; 34:2337-9.
• [22]Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M et al.. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011; 69:292-302.
• [23]Doering A, Pfueller CF, Paul F, Dörr J. Exercise in multiple sclerosis—an integral component of disease management. EPMA J. 2012; 3:2.
• [24]Dörr J, Doering A, Paul F. Can we prevent or treat multiple sclerosis by individualised vitamin D supply. EPMA J. 2013; 4:1-12.
• [25]Urbanek C, Weinges-Evers N, Bellmann-Strobl J, Bock M, Dorr J, Hahn E et al.. Attention Network Test reveals alerting network dysfunction in multiple sclerosis. Mult Scler J. 2010; 16:93-9.
• [26]Weinges-Evers N, Brandt AU, Bock M, Pfueller CF, Dorr J, Bellmann-Strobl J et al.. Correlation of self-assessed fatigue and alertness in multiple sclerosis. Mult Scler J. 2010; 16:1134-40.
• [27]Bellmann-Strobl J, Wuerfel J, Aktas O, Dörr J, Wernecke KD, Zipp F et al.. Poor PASAT performance correlates with MRI contrast enhancement in multiple sclerosis. Neurology. 2009; 73:1624-7.
• [28]Veauthier C, Paul F. Fatigue in multiple sclerosis: which patient should be referred to a sleep specialist? Mult Scler J. 2012; 18:248-9.
• [29]Finke C, Pech LM, Sömmer C, Schlichting J, Stricker S, Endres M et al.. Dynamics of saccade parameters in multiple sclerosis patients with fatigue. J Neurol. 2012; 259:2656-63.
• [30]Wieder L, Gäde G, Pech LM, Zimmermann H, Wernecke K-D, Dörr J et al.. Low contrast visual acuity testing is associated with cognitive performance in multiple sclerosis: a cross-sectional pilot study. BMC Neurol. 2013; 13:167.
• [31]Scheel M, Finke C, Oberwahrenbrock T, Freing A, Pech L, Schlichting J et al.. Retinal nerve fibre layer thickness correlates with brain white matter damage in multiple sclerosis: a combined optical coherence tomography and diffusion tensor imaging study. Mult Scler J. 2014; 20:190-7.
• [32]Zimmermann H, Freing A, Kaufhold F, Gaede G, Bohn E, Bock M et al.. Optic neuritis interferes with optical coherence tomography and magnetic resonance imaging correlations. Mult Scler J. 2013; 19:443-50.
• [33]Oberwahrenbrock T, Ringelstein M, Jentschke S, Deuschle K, Klumbies K, Bellmann-Strobl J et al.. Retinal ganglion cell and inner plexiform layer thinning in clinically isolated syndrome. Mult Scler J. 2013; 19:1887-95.
• [34]Bock M, Brandt AU, Kuchenbecker J, Dorr J, Pfueller CF, Weinges-Evers N et al.. Impairment of contrast visual acuity as a functional correlate of retinal nerve fibre layer thinning and total macular volume reduction in multiple sclerosis. Br J Ophthalmol. 2012; 96:62-7.
• [35]Bock M, Brandt AU, Dorr J, Pfueller CF, Ohlraun S, Zipp F et al.. Time domain and spectral domain optical coherence tomography in multiple sclerosis: a comparative cross-sectional study. Mult Scler J. 2010; 16:893-6.
• [36]Brandt AU, Oberwahrenbrock T, Ringelstein M, Young KL, Tiede M, Hartung HP et al.. Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain. 2011; 134: Article ID e193
• [37]Simon J. Very early MS—insights from MRI. Mult Scler J. 2012; 18:1372-6.
• [38]Londono AC, Mora CA. Nonconventional MRI biomarkers for in vivo monitoring of pathogenesis in multiple sclerosis. Neurol Neuroimmunol Neuroinflammation. 2014; 1: Article ID e45
• [39]Ciccarelli O, Barkhof F, Bodini B, De Stefano N, Golay X, Nicolay K et al.. Pathogenesis of multiple sclerosis: insights from molecular and metabolic imaging. Lancet Neurol. 2014; 13:807-22.
• [40]Huhn K, Lämmer R, Oberwahrenbrock T, Lämmer A, Waschbisch A, Gosar D et al.. Optical coherence tomography in patients with a history of juvenile multiple sclerosis reveals early retinal damage. Eur J Neurol. 2015; 22:86-92.
• [41]Finke C, Schlichting J, Papazoglou S, Scheel M, Freing A, Soemmer C et al.. Altered basal ganglia functional connectivity in multiple sclerosis patients with fatigue. Mult Scler J. 2015; 21:925-34.
• [42]Pfueller CF, Brandt AU, Schubert F, Bock M, Walaszek B, Waiczies H et al.. Metabolic changes in the visual cortex are linked to retinal nerve fiber layer thinning in multiple sclerosis. PLoS ONE. 2011; 6: Article ID e18019
• [43]Bellmann-Strobl J, Stiepani H, Wuerfel J, Bohner G, Paul F, Warmuth C et al.. MR spectroscopy (MRS) and magnetisation transfer imaging (MTI), lesion load and clinical scores in early relapsing remitting multiple sclerosis: a combined cross-sectional and longitudinal study. Eur Radiol. 2009; 19:2066-74.
• [44]Streitberger K-J, Sack I, Krefting D, Pfüller C, Braun J, Paul F et al.. Brain viscoelasticity alteration in chronic-progressive multiple sclerosis. PLoS ONE. 2012; 7: Article ID e29888
• [45]Charil A, Yousry TA, Rovaris M, Barkhof F, De Stefano N, Fazekas F et al.. MRI and the diagnosis of multiple sclerosis: expanding the concept of “no better explanation”. Lancet Neurol. 2006; 5:841-52.
• [46]Solomon AJ, Klein EP, Bourdette D. “Undiagnosing” multiple sclerosis: the challenge of misdiagnosis in MS. Neurology. 2012; 78:1986-91.
• [47]Hohlfeld R. “Gimme five”: future challenges in multiple sclerosis. ECTRIMS Lecture 2009. Mult Scler J. 2010; 16:3-14.
• [48]Dörr J, Bitsch A, Schmailzl KJG, Chan A, Von Ahsen N, Hummel M et al.. Severe cardiac failure in a patient with multiple sclerosis following low-dose mitoxantrone treatment. Neurology. 2009; 73:991-3.
• [49]Stroet A, Hemmelmann C, Starck M, Zettl U, Dörr J, Paul F et al.. Incidence of therapy-related acute leukaemia in mitoxantrone-treated multiple sclerosis patients in Germany. Ther Adv Neurol Disord. 2012; 5:75-9.
• [50]Dörr J, Paul F. The transition from first-line to second-line therapy in multiple sclerosis. Curr Treat Options Neurol. 2015; 17:354.
• [51]Borisow N, Doering A, Pfueller CF, Paul F, Dörr J, Hellwig K. Expert recommendations to personalization of medical approaches in treatment of multiple sclerosis: an overview of family planning and pregnancy. EPMA J. 2012; 3:9.
• [52]Li V, Kane J, Chan HH, Hall AJ, Butzkueven H. Continuing fingolimod after development of macular edema: a case report. Neurol-Neuroimmunol Neuroinflammation. 2014; 1: Article ID e13
• [53]Clausi V, Giannecchini S, Magnani E, Repice A, Mechi C, Martelli F et al.. Markers of JC virus infection in patients with multiple sclerosis under natalizumab therapy. Neurol Neuroimmunol Neuroinflammation. 2015; 2:e58-–8.
• [54]Vennegoor A, van Rossum JA, Polman CH, Wattjes MP, Killestein J. Longitudinal JCV serology in multiple sclerosis patients preceding natalizumab-associated progressive multifocal leukoencephalopathy. Mult Scler J. 2015.
• [55]Tallantyre EC, Morgan PS, Dixon JE, Al- RA, Brookes MJ, Morris PG et al.. 3 Tesla and 7 Tesla MRI of multiple sclerosis cortical lesions. J Magn Reson Imaging. 2010; 32:971-7.
• [56]Magliozzi R, Howell O, Vora A, Serafini B, Nicholas R, Puopolo M et al.. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain J Neurol. 2007; 130:1089-104.
• [57]Schmierer K, Parkes HG, So P-W, An SF, Brandner S, Ordidge RJ et al.. High field (9.4 Tesla) magnetic resonance imaging of cortical grey matter lesions in multiple sclerosis. Brain J Neurol. 2010; 133:858-67.
• [58]Kutzelnigg A, Lucchinetti CF, Stadelmann C, Brück W, Rauschka H, Bergmann M et al.. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain. 2005; 128:2705-12.
• [59]Calabrese M, Poretto V, Favaretto A, Alessio S, Bernardi V, Romualdi C et al.. Cortical lesion load associates with progression of disability in multiple sclerosis. Brain J Neurol. 2012; 135:2952-61.
• [60]DeLuca GC, Yates RL, Beale H, Morrow SA. Cognitive impairment in multiple sclerosis: clinical, radiologic and pathologic insights. Brain Pathol Zurich Switz. 2015; 25:79-98.
• [61]Nielsen AS, Kinkel RP, Madigan N, Tinelli E, Benner T, Mainero C. Contribution of cortical lesion subtypes at 7T MRI to physical and cognitive performance in MS. Neurology. 2013; 81:641-9.
• [62]Geurts JJG, Bö L, Pouwels PJW, Castelijns JA, Polman CH, Barkhof F. Cortical lesions in multiple sclerosis: combined postmortem MR imaging and histopathology. Am J Neuroradiol. 2005; 26:572-7.
• [63]Geurts JJG, Pouwels PJW, Uitdehaag BMJ, Polman CH, Barkhof F, Castelijns JA. Intracortical lesions in multiple sclerosis: improved detection with 3D double inversion-recovery MR imaging. Radiology. 2005; 236:254-60.
• [64]Yao B, Hametner S, van Gelderen P, Merkle H, Chen C, Lassmann H et al.. 7 Tesla magnetic resonance imaging to detect cortical pathology in multiple sclerosis. PloS One. 2014; 9: Article ID e108863
• [65]Abdel-Fahim R, Mistry N, Mougin O, Blazejewska A, Pitiot A, Retkute R et al.. Improved detection of focal cortical lesions using 7T magnetisation transfer imaging in patients with multiple sclerosis. Mult Scler Relat Disord. 2014; 3:258-65.
• [66]Kilsdonk ID, de Graaf WL, Soriano AL, Zwanenburg JJ, Visser F, Kuijer JPA et al.. Multicontrast MR imaging at 7T in multiple sclerosis: highest lesion detection in cortical gray matter with 3D-FLAIR. Am J Neuroradiol. 2013; 34:791-6.
• [67]de Graaf WL, Kilsdonk ID, Lopez-Soriano A, Zwanenburg JJM, Visser F, Polman CH et al.. Clinical application of multi-contrast 7-T MR imaging in multiple sclerosis: increased lesion detection compared to 3 T confined to grey matter. Eur Radiol. 2013; 23:528-40.
• [68]Sinnecker T, Mittelstaedt P, Dörr J, Pfueller CF, Harms L, Niendorf T et al.. Multiple sclerosis lesions and irreversible brain tissue damage: a comparative ultrahigh-field strength magnetic resonance imaging study. Arch Neurol. 2012; 69:739-45.
• [69]Nielsen AS, Kinkel RP, Tinelli E, Benner T, Cohen-Adad J, Mainero C. Focal cortical lesion detection in multiple sclerosis: 3 Tesla DIR versus 7 Tesla FLASH-T2. J Magn Reson Imaging. 2012; 35:537-42.
• [70]Peterson JW, Bö L, Mörk S, Chang A, Trapp BD. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol. 2001; 50:389-400.
• [71]Kollia K, Maderwald S, Putzki N, Schlamann M, Theysohn JM, Kraff O et al.. First clinical study on ultra-high-field MR imaging in patients with multiple sclerosis: comparison of 1.5T and 7T. Am J Neuroradiol. 2009; 30:699-702.
• [72]Mainero C, Benner T, Radding A, van der Kouwe A, Jensen R, Rosen BR et al.. In vivo imaging of cortical pathology in multiple sclerosis using ultra-high field MRI. Neurology. 2009; 73:941-8.
• [73]Pitt D, Boster A, Pei W, Wohleb E, Jasne A, Zachariah CR et al.. Imaging cortical lesions in multiple sclerosis with ultra-high-field magnetic resonance imaging. Arch Neurol. 2010; 67:812-8.
• [74]Metcalf M, Xu D, Okuda DT, Carvajal L, Srinivasan R, Kelley DAC et al.. High-resolution phased-array MRI of the human brain at 7 tesla: initial experience in multiple sclerosis patients. J Neuroimaging. Off J Am Soc Neuroimaging. 2010; 20:141-7.
• [75]Fischer MT, Wimmer I, Höftberger R, Gerlach S, Haider L, Zrzavy T et al.. Disease-specific molecular events in cortical multiple sclerosis lesions. Brain J Neurol. 2013; 136:1799-815.
• [76]Cohen-Adad J, Benner T, Greve D, Kinkel RP, Radding A, Fischl B et al.. In vivo evidence of disseminated subpial T2* signal changes in multiple sclerosis at 7 T: a surface-based analysis. NeuroImage. 2011; 57:55-62.
• [77]Harrison DM, Oh J, Roy S, Wood ET, Whetstone A, Seigo MA, et al. Thalamic lesions in multiple sclerosis by 7T MRI: clinical implications and relationship to cortical pathology. Mult Scler J. 2015. doi:10.117/1352458514558134.
• [78]van Walderveen MA, Barkhof F, Hommes OR, Polman CH, Tobi H, Frequin ST et al.. Correlating MRI and clinical disease activity in multiple sclerosis: relevance of hypointense lesions on short-TR/short-TE (T1-weighted) spin-echo images. Neurology. 1995; 45:1684-90.
• [79]Sailer M, Losseff NA, Wang L, Gawne-Cain ML, Thompson AJ, Miller DH. T1 lesion load and cerebral atrophy as a marker for clinical progression in patients with multiple sclerosis. A prospective 18 months follow-up study. Eur J Neurol Off J Eur Fed Neurol Soc. 2001; 8:37-42.
• [80]Mistry N, Tallantyre EC, Dixon JE, Galazis N, Jaspan T, Morgan PS et al.. Focal multiple sclerosis lesions abound in “normal appearing white matter”. Mult Scler J. 2011; 17:1313-23.
• [81]Tallantyre EC, Morgan PS, Dixon JE, Al- RA, Brookes MJ, Evangelou N et al.. A comparison of 3T and 7T in the detection of small parenchymal veins within MS lesions. Invest Radiol. 2009; 44:491-4.
• [82]Tallantyre EC, Brookes MJ, Dixon JE, Morgan PS, Evangelou N, Morris PG. Demonstrating the perivascular distribution of MS lesions in vivo with 7-Tesla MRI. Neurology. 2008; 70:2076-8.
• [83]Kuchling J, Ramien C, Bozin I, Dörr J, Harms L, Rosche B et al.. Identical lesion morphology in primary progressive and relapsing-remitting MS—an ultrahigh field MRI study. Mult Scler J. 2014; 20:1866-71.
• [84]Absinta M, Sati P, Gaitán MI, Maggi P, Cortese ICM, Filippi M et al.. Seven-tesla phase imaging of acute multiple sclerosis lesions: a new window into the inflammatory process. Ann Neurol. 2013; 74:669-78.
• [85]Bian W, Harter K, Hammond-Rosenbluth KE, Lupo JM, Xu D, Kelley DA et al.. A serial in vivo 7T magnetic resonance phase imaging study of white matter lesions in multiple sclerosis. Mult Scler J. 2013; 19:69-75.
• [86]Radaideh AM A, Wharton SJ, Lim S-Y, Tench CR, Morgan PS, Bowtell RW et al.. Increased iron accumulation occurs in the earliest stages of demyelinating disease: an ultra-high field susceptibility mapping study in Clinically Isolated Syndrome. Mult Scler J. 2013; 19:896-903.
• [87]Hametner S, Wimmer I, Haider L, Pfeifenbring S, Brück W, Lassmann H. Iron and neurodegeneration in the multiple sclerosis brain. Ann Neurol. 2013; 74:848-61.
• [88]Bagnato F, Hametner S, Yao B, van Gelderen P, Merkle H, Cantor FK et al.. Tracking iron in multiple sclerosis: a combined imaging and histopathological study at 7 Tesla. Brain J Neurol. 2011; 134:3602-15.
• [89]Adams CW. Perivascular iron deposition and other vascular damage in multiple sclerosis. J Neurol Neurosurg Psychiatry. 1988; 51:260-5.
• [90]Bozin I, Ge Y, Kuchling J, Dusek P, Chawla S, Harms L, et al. Magnetic resonance phase alterations in multiple sclerosis patients with short and long disease duration. PLoS One. 2015;10(7):e0128386.
• [91]Connor JR, Menzies SL. Relationship of iron to oligodendrocytes and myelination. Glia. 1996; 17:83-93.
• [92]Sinnecker T, Dörr J, Pfueller CF, Harms L, Ruprecht K, Jarius S et al.. Distinct lesion morphology at 7-T MRI differentiates neuromyelitis optica from multiple sclerosis. Neurology. 2012; 79:708-14.
• [93]Kister I, Herbert J, Zhou Y, Ge Y. Ultrahigh-field MR (7 T) imaging of brain lesions in neuromyelitis optica. Mult Scler Int. 2013.
• [94]Tallantyre EC, Dixon JE, Donaldson I, Owens T, Morgan PS, Morris PG et al.. Ultra-high-field imaging distinguishes MS lesions from asymptomatic white matter lesions. Neurology. 2011; 76:534-9.
• [95]Wuerfel J, Sinnecker T, Ringelstein EB, Jarius S, Schwindt W, Niendorf T et al.. Lesion morphology at 7 Tesla MRI differentiates Susac syndrome from multiple sclerosis. Mult Scler J. 2012; 18:1592-9.
• [96]Mistry N, Dixon J, Tallantyre E, Tench C, Abdel-Fahim R, Jaspan T et al.. Central veins in brain lesions visualized with high-field magnetic resonance imaging: a pathologically specific diagnostic biomarker for inflammatory demyelination in the brain. JAMA Neurol. 2013; 70:623-8.
• [97]Paul F, Wattjes MP. Chronic cerebrospinal venous insufficiency in multiple sclerosis: the final curtain. Lancet. 2014; 383:106-8.
• [98]Valdueza JM, Doepp F, Schreiber SJ, van Oosten BW, Schmierer K, Paul F et al.. What went wrong? The flawed concept of cerebrospinal venous insufficiency. J Cereb Blood Flow Metab. 2013; 33:657-68.
• [99]Doepp F, Paul F, Valdueza JM, Schmierer K, Schreiber SJ. No cerebrocervical venous congestion in patients with multiple sclerosis. Ann Neurol. 2010; 68:173-83.
• [100]Doepp F, Wuerfel JT, Pfueller CF, Valdueza JM, Petersen D, Paul F et al.. Venous drainage in multiple sclerosis: a combined MRI and ultrasound study. Neurology. 2011; 77:1745-51.
• [101]Dawson J. The histology of disseminated sclerosis. Trans Roy Soc Edin. 1916;50:517-740.
• [102]Müller K, Kuchling J, Dörr J, Harms L, Ruprecht K, Niendorf T et al.. Detailing intra-lesional venous lumen shrinking in multiple sclerosis investigated by sFLAIR MRI at 7-T. J Neurol. 2014; 261:2032-6.
• [103]Sinnecker T, Bozin I, Dörr J, Pfueller CF, Harms L, Niendorf T et al.. Periventricular venous density in multiple sclerosis is inversely associated with T2 lesion count: a 7 Tesla MRI study. Mult Scler J. 2013; 19:316-25.
• [104]Gaitán MI, de Alwis MP, Sati P, Nair G, Reich DS. Multiple sclerosis shrinks intralesional, and enlarges extralesional, brain parenchymal veins. Neurology. 2013; 80:145-51.
• [105]Adams CW, Poston RN, Buk SJ, Sidhu YS, Vipond H. Inflammatory vasculitis in multiple sclerosis. J Neurol Sci. 1985; 69:269-83.
• [106]Sinnecker T, Oberwahrenbrock T, Metz I, Zimmermann H, Pfueller CF, Harms L et al.. Optic radiation damage in multiple sclerosis is associated with visual dysfunction and retinal thinning—an ultrahigh-field MR pilot study. Eur Radiol. 2014; 25:122-31.
• [107]Marques JP, Kober T, Krueger G, van der Zwaag W, Van de Moortele P-F, Gruetter R. MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field. NeuroImage. 2010; 49:1271-81.
• [108]Fujimoto K, Polimeni JR, van der Kouwe AJW, Reuter M, Kober T, Benner T et al.. Quantitative comparison of cortical surface reconstructions from MP2RAGE and multi-echo MPRAGE data at 3 and 7 T. NeuroImage. 2014; 90:60-73.
• [109]Seiger R, Hahn A, Hummer A, Kranz GS, Ganger S, Küblböck M et al.. Voxel-based morphometry at ultra-high fields. A comparison of 7T and 3T MRI data. NeuroImage. 2015; 113:207-16.
• [110]O’Brien KR, Kober T, Hagmann P, Maeder P, Marques J, Lazeyras F et al.. Robust T1-weighted structural brain imaging and morphometry at 7T using MP2RAGE. PloS One. 2014; 9: Article ID e99676
• [111]Jarius S, Ruprecht K, Wildemann B, Kuempfel T, Ringelstein M, Geis C et al.. Contrasting disease patterns in seropositive and seronegative neuromyelitis optica: a multicentre study of 175 patients. J Neuroinflammation. 2012; 9:14.
• [112]Jarius S, Wildemann B, Paul F. Neuromyelitis optica: clinical features, immunopathogenesis and treatment. Clin Exp Immunol. 2014; 176:149-64.
• [113]Lucchinetti CF, Mandler RN, McGavern D, Bruck W, Gleich G, Ransohoff RM et al.. A role for humoral mechanisms in the pathogenesis of Devic’s neuromyelitis optica. Brain. 2002; 125:1450-61.
• [114]Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR. IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med. 2005; 202:473-7.
• [115]Jarius S, Franciotta D, Paul F, Bergamaschi R, Rommer PS, Ruprecht K et al.. Testing for antibodies to human aquaporin-4 by ELISA: sensitivity, specificity, and direct comparison with immunohistochemistry. J Neurol Sci. 2012; 320:32-7.
• [116]Jarius S, Paul F, Fechner K, Ruprecht K, Kleiter I, Franciotta D et al.. Aquaporin-4 antibody testing: direct comparison of M1-AQP4-DNA-transfected cells with leaky scanning versus M23-AQP4-DNA-transfected cells as antigenic substrate. J Neuroinflammation. 2014; 11:129.
• [117]Kister I, Paul F. Pushing the boundaries of neuromyelitis optica: does antibody make the disease? Neurology. 2015.
• [118]Hertwig L, Pache F, Romero-Suarez S, Stürner KH, Borisow N, Behrens J et al.. Distinct functionality of neutrophils in multiple sclerosis and neuromyelitis optica. Mult Scler J. 2015.
• [119]Jarius S, Paul F, Franciotta D, Waters P, Zipp F, Hohlfeld R et al.. Mechanisms of disease: aquaporin-4 antibodies in neuromyelitis optica. Nat Clin Pract Neurol. 2008; 4:202-14.
• [120]Paul F, Jarius S, Aktas O, Bluthner M, Bauer O, Appelhans H et al.. Antibody to aquaporin 4 in the diagnosis of neuromyelitis optica. PLoS Med. 2007; 4:669.
• [121]Bennett JL, de Seze J, Lana-Peixoto M, Palace J, Waldman A, Schippling S et al.. Neuromyelitis optica and multiple sclerosis: seeing differences through optical coherence tomography. Mult Scler J. 2015; 21:678-88.
• [122]Schneider E, Zimmermann H, Oberwahrenbrock T, Kaufhold F, Kadas EM, Petzold A et al.. Optical coherence tomography reveals distinct patterns of retinal damage in neuromyelitis optica and multiple sclerosis. PLoS ONE. 2013; 8: Article ID e66151
• [123]Shimizu J, Hatanaka Y, Hasegawa M, Iwata A, Sugimoto I, Date H et al.. IFNβ-1b may severely exacerbate Japanese optic-spinal MS in neuromyelitis optica spectrum. Neurology. 2010; 75:1423-7.
• [124]Cree Ba C, Lamb S, Morgan K, Chen A, Waubant E, Genain C. An open label study of the effects of rituximab in neuromyelitis optica. Neurology. 2005; 64:1270-2.
• [125]Kleiter I, Hellwig K, Berthele A, Kümpfel T, Linker RA, Hartung H-P et al.. Failure of natalizumab to prevent relapses in neuromyelitis optica. Arch Neurol. 2012; 69:239-45.
• [126]Trebst C, Jarius S, Berthele A, Paul F, Schippling S, Wildemann B et al.. Update on the diagnosis and treatment of neuromyelitis optica: recommendations of the Neuromyelitis Optica Study Group (NEMOS). J Neurol. 2014; 261:1-16.
• [127]Min J-H, Kim BJ, Lee KH. Development of extensive brain lesions following fingolimod (FTY720) treatment in a patient with neuromyelitis optica spectrum disorder. Mult Scler J. 2012; 18:113-5.
• [128]Jarernsook B, Siritho S, Prayoonwiwat N. Efficacy and safety of beta-interferon in Thai patients with demyelinating diseases. Mult Scler J. 2012; 19:585-92.
• [129]Pittock SJ, Lennon VA, Krecke K, Wingerchuk DM, Lucchinetti CF, Weinshenker BG. Brain abnormalities in neuromyelitis optica. Arch Neurol. 2006; 63:390-6.
• [130]Matthews L, Marasco R, Jenkinson M, Küker W, Luppe S, Leite MI et al.. Distinction of seropositive NMO spectrum disorder and MS brain lesion distribution. Neurology. 2013; 80:1330-7.
• [131]Kim HJ, Paul F, Lana-Peixoto MA, Tenembaum S, Asgari N, Palace J et al.. MRI characteristics of neuromyelitis optica spectrum disorder: an international update. Neurology. 2015; 84:1165-73.
• [132]Flanagan EP, Weinshenker BG, Krecke KN, Lennon VA, Lucchinetti CF, McKeon A et al.. Short myelitis lesions in aquaporin-4-IgG-positive neuromyelitis optica spectrum disorders. JAMA Neurol. 2015; 72:81.
• [133]Susac JO, Hardman JM, Selhorst JB. Microangiopathy of the brain and retina. Neurology. 1979; 29:313-316.
• [134]Susac JO. Susac’s syndrome: the triad of microangiopathy of the brain and retina with hearing loss in young women. Neurology. 1994; 44:591-593.
• [135]Dörr J, Radbruch H, Bock M, Wuerfel J, Brüggemann A, Wandinger KP et al.. Encephalopathy, visual disturbance and hearing loss-recognizing the symptoms of Susac syndrome. Nat Rev Neurol. 2009; 5:683-8.
• [136]Dörr J, Krautwald S, Wildemann B, Jarius S, Ringelstein M, Duning T et al.. Characteristics of Susac syndrome: a review of all reported cases. Nat Rev Neurol. 2013; 9:307-16.
• [137]Jarius S, Kleffner I, Dörr JM, Sastre-Garriga J, Illes Z, Eggenberger E et al.. Clinical, paraclinical and serological findings in Susac syndrome: an international multicenter study. J Neuroinflammation. 2014; 11:46.
• [138]Brandt AU, Zimmermann H, Kaufhold F, Promesberger J, Schippling S, Finis D et al.. Patterns of retinal damage facilitate differential diagnosis between Susac syndrome and MS. PLoS ONE. 2012; 7: Article ID e38741
• [139]Ringelstein M, Albrecht P, Kleffner I, Bühn B, Harmel J, Müller A, et al. Retinal pathology in Susac syndrome detected by spectral-domain optical coherence tomography. Neurology. 2015;85(7):610-8.
• [140]Dörr J, Jarius S, Wildemann B, Ringelstein EB, Schwindt W, Deppe M et al.. Susac syndrome: an interdisciplinary challenge. Nervenarzt. 2011; 82:1250-63.
• [141]Dörr J, Ringelstein M, Duning T, Kleffner I. Update on Susac syndrome: new insights in brain and retinal imaging and treatment options. J Alzheimers Dis. 2014; 42 Suppl 3:S99-108.
• [142]Rennebohm RM, Egan RA, Susac JO. Treatment of Susac’s Syndrome. Curr Treat Options Neurol. 2008; 10:67-74.
• [143]Saux A, Niango G, Charif M, Morales R, Mura F, Bonafe A et al.. Susac’s syndrome, a rare, potentially severe or lethal neurological disease. J Neurol Sci. 2010; 297:71-3.
• [144]Susac JO, Murtagh FR, Egan RA, Berger JR, Bakshi R, Lincoff N et al.. MRI findings in Susac’s syndrome. Neurology. 2003; 61:1783-7.
• [145]Kilsdonk ID, Wattjes MP, Lopez-Soriano A, Kuijer JPA, de Jong MC, de Graaf WL et al.. Improved differentiation between MS and vascular brain lesions using FLAIR* at 7 Tesla. Eur Radiol. 2014; 24:841-9.
• [146]Sati P, George IC, Shea CD, Gaitán MI, Reich DS. FLAIR*: a combined MR contrast technique for visualizing white matter lesions and parenchymal veins. Radiology. 2012; 265:926-32.
• [147]Grabner G, Dal-Bianco A, Schernthaner M, Vass K, Lassmann H, Trattnig S. 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; 33:543-9.
• [148]Dixon JE, Simpson A, Mistry N, Evangelou N, Morris PG. Optimisation of T2*-weighted MRI for the detection of small veins in multiple sclerosis at 3 T and 7 T. Eur J Radiol. 2013; 82:719-27.