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Neuromyelitis optica does not impact periventricular venous density versus healthy controls: a 7.0 Tesla MRI clinical study

  • Sophie Schumacher
  • Florence Pache
  • Judith Bellmann-Strobl
  • Janina Behrens
  • Petr Dusek
  • Lutz Harms
  • Klemens Ruprecht
  • Petra Nytrova
  • Sanjeev Chawla
  • Thoralf Niendorf
  • Ilya Kister
  • Friedemann Paul
  • Yulin Ge
  • Jens Wuerfel
  • Tim Sinnecker
Research Article

Abstract

Objective

To quantify the periventricular venous density in neuromyelitis optica spectrum disease (NMOSD) in comparison to that in patients with multiple sclerosis (MS) and healthy control subjects.

Materials and methods

Sixteen patients with NMOSD, 16 patients with MS and 16 healthy control subjects underwent 7.0-Tesla (7T) MRI. The imaging protocol included T2*-weighted (T2*w) fast low angle-shot (FLASH) and fluid-attenuated inversion recovery (FLAIR) sequences. The periventricular venous area (PVA) was manually determined by a blinded investigator in order to estimate the periventricular venous density in a region of interest-based approach.

Results

No significant differences in periventricular venous density indicated by PVA were detectable in NMOSD versus healthy controls (p = 0.226). In contrast, PVA was significantly reduced in MS patients compared to healthy controls (p = 0.013).

Conclusion

Unlike patients with MS, those suffering from NMOSD did not show reduced venous visibility. This finding may underscore primary and secondary pathophysiological differences between these two distinct diseases of the central nervous system.

Keywords

Ultrahigh-field MRI 7T MRI Multiple sclerosis Neuromyelitis optica Venous density 

Notes

Acknowledgments

This work was supported by the Guthy-Jackson Charitable Foundation, the German Research Foundation (DFG Exc 257 to FP) and the German Ministry for Education and Research (Competence Network Multiple Sclerosis) to FP, FlP, JW and KR. Our technicians and study nurses Antje Els, Susan Pikol, Cynthia Kraut and Gritt Stoffels gave invaluable support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

10334_2016_554_MOESM1_ESM.tif (6.6 mb)
Supplementary material 1 (TIFF 6,803 kb)

References

  1. 1.
    Wingerchuk DM, Banwell B, Bennett JL, Cabre P, Carroll W, Chitnis T, de Seze J, Fujihara K, Greenberg B, Jacob A, Jarius S, Lana-Peixoto M, Levy M, Simon JH, Tenembaum S, Traboulsee AL, Waters P, Wellik KE, Weinshenker BG, International Panel for NMO Diagnosis (2015) International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 85:177–189CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Kim HJ, Paul F, Lana-Peixoto MA, Tenembaum S, Asgari N, Palace J, Klawiter EC, Sato DK, de Seze J, Wuerfel J, Banwell BL, Villoslada P, Saiz A, Fujihara K, Kim S-H, Guthy-Jackson Charitable Foundation NMO International Clinical Consortium and Biorepository (2015) MRI characteristics of neuromyelitis optica spectrum disorder: an international update. Neurology 84:1165–1173CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Jarius S, Wildemann B, Paul F (2014) Neuromyelitis optica: clinical features, immunopathogenesis and treatment. Clin Exp Immunol 176:149–164CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Kleiter I, Gahlen A, Borisow N, Fischer K, Wernecke K-D, Wegner B, Hellwig K, Pache F, Ruprecht K, Havla J, Krumbholz M, Kümpfel T, Aktas O, Hartung H-P, Ringelstein M, Geis C, Kleinschnitz C, Berthele A, Hemmer B, Angstwurm K, Stellmann J-P, Schuster S, Stangel M, Lauda F, Tumani H, Mayer C, Zeltner L, Ziemann U, Linker R, Schwab M, Marziniak M, Bergh FT, Hofstadt-van Oy U, Neuhaus O, Winkelmann A, Marouf W, Faiss J, Wildemann B, Paul F, Jarius S, Trebst C, NEMOS (Neuromyelitis Optica Study Group) (2015) Neuromyelitis optica: Evaluation of 871 attacks and 1153 treatment courses. Ann Neurol 79:206–216CrossRefPubMedGoogle Scholar
  5. 5.
    Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR (2005) IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med 202:473–477CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Paul F, Jarius S, Aktas O, Bluthner M, Bauer O, Appelhans H, Franciotta D, Bergamaschi R, Littleton E, Palace J, Seelig H-P, Hohlfeld R, Vincent A, Zipp F (2007) Antibody to aquaporin 4 in the diagnosis of neuromyelitis optica. PLoS Med 4:e133CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Jarius S, Ruprecht K, Wildemann B, Kuempfel T, Ringelstein M, Geis C, Kleiter I, Kleinschnitz C, Berthele A, Brettschneider J, Hellwig K, Hemmer B, Linker RA, Lauda F, Mayer CA, Tumani H, Melms A, Trebst C, Stangel M, Marziniak M, Hoffmann F, Schippling S, Faiss JH, Neuhaus O, Ettrich B, Zentner C, Guthke K, Hofstadt-van Oy U, Reuss R, Pellkofer H, Ziemann U, Kern P, Wandinger KP, Bergh FT, Boettcher T, Langel S, Liebetrau M, Rommer PS, Niehaus S, Münch C, Winkelmann A, Zettl UUK, Metz I, Veauthier C, Sieb JP, Wilke C, Hartung HP, Aktas O, Paul F (2012) Contrasting disease patterns in seropositive and seronegative neuromyelitis optica: a multicentre study of 175 patients. J Neuroinflammation 9:14CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Trebst C, Jarius S, Berthele A, Paul F, Schippling S, Wildemann B, Borisow N, Kleiter I, Aktas O, Kümpfel T, Neuromyelitis Optica Study Group (NEMOS) (2014) Update on the diagnosis and treatment of neuromyelitis optica: recommendations of the Neuromyelitis Optica Study Group (NEMOS). J Neurol 261:1–16CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Reichenbach JR, Venkatesan R, Schillinger DJ, Kido DK, Haacke EM (1997) Small vessels in the human brain: MR venography with deoxyhemoglobin as an intrinsic contrast agent. Radiology 204:272–277CrossRefPubMedGoogle Scholar
  10. 10.
    Tallantyre EC, Morgan PS, Dixon JE, Al-Radaideh A, Brookes MJ, Evangelou N, Morris PG (2009) A comparison of 3T and 7 T in the detection of small parenchymal veins within MS lesions. Invest Radiol 44:491–494CrossRefPubMedGoogle Scholar
  11. 11.
    Sinnecker T, Kuchling J, Dusek P, Dörr J, Niendorf T, Paul F, Wuerfel J (2015) Ultrahigh field MRI in clinical neuroimmunology: a potential contribution to improved diagnostics and personalised disease management. EPMA J 6:16CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Sinnecker T, Dörr J, Pfueller CF, Harms L, Ruprecht K, Jarius S, Brück W, Niendorf T, Wuerfel J, Paul F (2012) Distinct lesion morphology at 7-T MRI differentiates neuromyelitis optica from multiple sclerosis. Neurology 79:708–714CrossRefPubMedGoogle Scholar
  13. 13.
    Kister I, Herbert J, Zhou Y, Ge Y (2013) Ultrahigh-Field MR (7 T) Imaging of Brain Lesions in Neuromyelitis Optica. Mult Scler Int 2013:398259PubMedPubMedCentralGoogle Scholar
  14. 14.
    Sinnecker T, Bozin I, Dörr J, Pfueller CF, Harms L, Niendorf T, Brandt AU, Paul F, Wuerfel J (2013) Periventricular venous density in multiple sclerosis is inversely associated with T 2 lesion count: a 7 T MRI study. Mult Scler 19:316–325CrossRefPubMedGoogle Scholar
  15. 15.
    Ge Y, Zohrabian VM, Osa E-O, Xu J, Jaggi H, Herbert J, Haacke EM, Grossman RI (2009) Diminished visibility of cerebral venous vasculature in multiple sclerosis by susceptibility-weighted imaging at 3.0 T. J Magn Reson Imaging 29:1190–1194CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O’Connor P, Sandberg-Wollheim M, Thompson AJ, Waubant E, Weinshenker B, Wolinsky JS (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69:292–302CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33:1444–1452CrossRefPubMedGoogle Scholar
  18. 18.
    Ge Y, Zhang Z, Lu H, Tang L, Jaggi H, Herbert J, Babb JS, Rusinek H, Grossman RI (2012) Characterizing brain oxygen metabolism in patients with multiple sclerosis with T 2-relaxation-under-spin-tagging MRI. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab 32:403–412CrossRefGoogle Scholar
  19. 19.
    Adams CW (1988) Perivascular iron deposition and other vascular damage in multiple sclerosis. J Neurol Neurosurg Psychiatry 51:260–265CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Wuerfel J, Paul F, Zipp F (2007) Cerebral blood perfusion changes in multiple sclerosis. J Neurol Sci 259:16–20CrossRefPubMedGoogle Scholar
  21. 21.
    Kimura MCG, Doring TM, Rueda FC, Tukamoto G, Gasparetto EL (2014) In vivo assessment of white matter damage in neuromyelitis optica: a diffusion tensor and diffusion kurtosis MR imaging study. J Neurol Sci 345:172–175CrossRefPubMedGoogle Scholar
  22. 22.
    Aboul-Enein F, Krssák M, Höftberger R, Prayer D, Kristoferitsch W (2010) Diffuse white matter damage is absent in neuromyelitis optica. AJNR Am J Neuroradiol 31:76–79CrossRefPubMedGoogle Scholar
  23. 23.
    Liu Y, Wang J, Daams M, Weiler F, Hahn HK, Duan Y, Huang J, Ren Z, Ye J, Dong H, Vrenken H, Wattjes MP, Shi F-D, Li K, Barkhof F (2015) Differential patterns of spinal cord and brain atrophy in NMO and MS. Neurology 84:1465–1472CrossRefPubMedGoogle Scholar
  24. 24.
    Jeantroux J, Kremer S, Lin XZ, Collongues N, Chanson J-B, Bourre B, Fleury M, Blanc F, Dietemann J-L, de Seze J (2012) Diffusion tensor imaging of normal-appearing white matter in neuromyelitis optica. J Neuroradiol 39:295–300CrossRefPubMedGoogle Scholar
  25. 25.
    Kremer S, Renard F, Achard S, Lana-Peixoto MA, Palace J, Asgari N, Klawiter EC, Tenembaum SN, Banwell B, Greenberg BM, Bennett JL, Levy M, Villoslada P, Saiz A, Fujihara K, Chan KH, Schippling S, Paul F, Kim HJ, de Seze J, Wuerfel JT, Guthy-Jackson Charitable Foundation (GJCF) Neuromyelitis Optica (NMO) International Clinical Consortium and Biorepository, Cabre P, Marignier R, Tedder T, van Pelt D, Broadley S, Chitnis T, Wingerchuk D, Pandit L, Leite MI, Apiwattanakul M, Kleiter I, Prayoonwiwat N, Han M, Hellwig K, van Herle K, John G, Hooper DC, Nakashima I, Sato D, Yeaman MR, Waubant E, Zamvil S, Stüve O, Aktas O, Smith TJ, Jacob A, O’Connor K (2015) Use of advanced magnetic resonance imaging techniques in neuromyelitis optica spectrum disorder. JAMA Neurol 72:815–822CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Von Glehn F, Jarius S, Cavalcanti Lira RP, Alves Ferreira MC, von Glehn FHR, Costa E, Castro SM, Beltramini GC, Bergo FP, Farias AS, Brandão CO, Wildemann B, Damasceno BP, Cendes F, Santos LMB, Yasuda CL (2014) Structural brain abnormalities are related to retinal nerve fiber layer thinning and disease duration in neuromyelitis optica spectrum disorders. Mult Scler. doi: 10.1177/1352458513519838 Google Scholar

Copyright information

© ESMRMB 2016

Authors and Affiliations

  • Sophie Schumacher
    • 1
  • Florence Pache
    • 1
    • 3
  • Judith Bellmann-Strobl
    • 1
    • 7
  • Janina Behrens
    • 1
  • Petr Dusek
    • 2
    • 3
  • Lutz Harms
    • 4
    • 5
  • Klemens Ruprecht
    • 4
    • 5
  • Petra Nytrova
    • 3
  • Sanjeev Chawla
    • 8
  • Thoralf Niendorf
    • 6
    • 7
  • Ilya Kister
    • 9
  • Friedemann Paul
    • 1
    • 4
    • 5
    • 7
  • Yulin Ge
    • 8
  • Jens Wuerfel
    • 1
    • 2
    • 6
    • 7
    • 10
  • Tim Sinnecker
    • 1
    • 10
    • 11
    • 12
  1. 1.NeuroCure Clinical Research CenterCharité-Universitätsmedizin BerlinBerlinGermany
  2. 2.Institute of NeuroradiologyUniversitätsmedizin GöttingenGöttingenGermany
  3. 3.Department of Neurology and Center of Clinical Neuroscience1st Faculty of Medicine, General University Hospital in Prague, Charles University in PraguePragueCzech Republic
  4. 4.Clinical and Experimental Multiple Sclerosis Research CenterCharité-Universitätsmedizin BerlinBerlinGermany
  5. 5.Department of NeurologyCharité-Universitätsmedizin BerlinBerlinGermany
  6. 6.Berlin Ultrahigh Field Facility (B.U.F.F.), Max Delbrück Center for Molecular MedicineBerlinGermany
  7. 7.Experimental and Clinical Research CenterCharité-Universitätsmedizin Berlin and Max Delbrück Center for Molecular MedicineBerlinGermany
  8. 8.Department of RadiologyNYU School of MedicineNew YorkUSA
  9. 9.Department of Neurology, Multiple Sclerosis Care CenterNYU School of MedicineNew YorkUSA
  10. 10.Medical Image Analysis Center AG (MIAC)BaselSwitzerland
  11. 11.Department of NeurologyAsklepios Fachklinikum TeupitzTeupitzGermany
  12. 12.Department of NeurologyUniversitätsspital BaselBaselSwitzerland

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