European Radiology

, Volume 23, Issue 3, pp 869–878 | Cite as

Cerebral vein changes in relapsing-remitting multiple sclerosis demonstrated by three-dimensional enhanced T 2 * -weighted angiography at 3.0 T

  • Chun Zeng
  • Xuan Chen
  • Yongmei Li
  • Yu Ouyang
  • Fajin Lv
  • Reshiana Rumzan
  • Zhongping Wang



To investigate characteristics of the internal cerebral veins (ICVs) and their main tributaries and the deep medullary veins (DMVs) in patients with relapsing-remitting MS (RRMS) with enhanced T 2 * -weighted angiography imaging (ESWAN).


Fifty-three RRMS patients and 53 normal controls underwent conventional MRI and ESWAN. ESWAN venograms were created by performing minimum intensity projections of the phase images, and the resulting venograms were used to observe characteristic vascular changes, including scores of the ICVs and their main tributaries and manifestations of the DMVs. Two experienced radiologists analysed all data.


Patients showed decreased mean scores of the ICVs and their main tributaries compared with controls. The mean score in acute patients was higher than in stable patients. Furthermore, the DMVs diminished and shortened in 48 patients with longer disease duration, whereas the DMVs increased and elongated in 5 patients with shorter disease duration. The penetrating veins were well defined in 30 active lesions, whereas the veins were ill defined in 69 non-active lesions. Interestingly, well-defined penetrating veins were shown in 15 non-active lesions in the stable patients.


Enhanced T 2 * -weighted MR angiography can detect cerebral vein characteristics in relapsing-remitting MS patients, which may provide important information on the pathogenesis of MS.

Key Points

Enhanced T 2 * -weighted magnetic resonance angiography (ESWAN) provides new insights into multiple sclerosis

ESWAN venograms clearly demonstrate the internal cerebral and deep medullary veins

The internal cerebral veins exhibit abnormalities in patients with relapsing-remitting MS

Deep medullary veins exhibit different manifestations in patients with different disease duration


Internal cerebral veins Deep medullary veins Relapsing-remitting multiple sclerosis Magnetic resonance imaging Three-dimensional enhanced T2*-weighted angiography 



The authors would like to thank Dexiang Yang for her assistance in data processing. We also thank all subjects for their cooperation and help. This work was supported by the National Natural Science Foundation of China (grant number 81171309), the Chongqing Municipal Natural Science Foundation of China (grant number CSTC2011JJA1073), the Medicine Key Scientific Research Project of Chongqing Health Bureau (grant number 2011-1-031) and the Medicine Scientific Research Project of Chongqing Health Bureau (grant number 2010-2-004).

C. Zeng and X. Chen contributed equally to this work.


  1. 1.
    Anderson VM, Wheeler-Kingshott CA, Abdel-Aziz K et al (2011) A comprehensive assessment of cerebellar damage in multiple sclerosis using diffusion tractography and volumetric analysis. Mult Scler 17:1079–1087PubMedCrossRefGoogle Scholar
  2. 2.
    Lassmann H, Brück W, Lucchinetti CF (2007) The immunopathology of multiple sclerosis: an overview. Brain Pathol 17:210–218PubMedCrossRefGoogle Scholar
  3. 3.
    de Graaf WL, Zwanenburg JJ, Visser F et al (2012) Lesion detection at seven Tesla in multiple sclerosis using magnetisation prepared 3D-FLAIR and 3D-DIR. Eur Radiol 22:221–231PubMedCrossRefGoogle Scholar
  4. 4.
    Simon B, Schmidt S, Lukas C et al (2010) Improved in vivo detection of cortical lesions in multiple sclerosis using double inversion recovery MR imaging at 3 Tesla. Eur Radiol 20:1675–1683PubMedCrossRefGoogle Scholar
  5. 5.
    Hohlfeld R (1997) Biotechnological agents for the immunotherapy of multiple sclerosis. Principles, problems and perspectives. Brain 120:865–916PubMedCrossRefGoogle Scholar
  6. 6.
    Ge Y, Law M, Herbert J, Grossman RI (2005) Prominent perivenular spaces in multiple sclerosis as a sign of perivascular inflammation in primary demyelination. AJNR Am J Neuroradiol 26:2316–2319PubMedGoogle Scholar
  7. 7.
    Kermode AG, Thompson AJ, Tofts P et al (1990) Breakdown of the blood–brain barrier precedes symptoms and other MRI signs of new lesions in multiple sclerosis. Pathogenetic and clinical implications. Brain 113:1477–1489PubMedCrossRefGoogle Scholar
  8. 8.
    Tan IL, van Schijnde RA, Pouwels PJ et al (2000) MR venography of multiple sclerosis. AJNR Am J Neuroradiol 21:1039–1042PubMedGoogle Scholar
  9. 9.
    Ge Y, Zohrabian VM, Grossman RI (2008) Seven-Tesla magnetic resonance imaging. New vision of microvascular abnormalities in multiple sclerosis. Arch Neurol 65:812–816PubMedCrossRefGoogle Scholar
  10. 10.
    Haacke EM, Makki M, Yulin G et al (2009) Characterizing iron deposition in multiple sclerosis lesions using susceptibility weighted imaging. J Magn Reson Imaging 29:537–544PubMedCrossRefGoogle Scholar
  11. 11.
    Putnam TJ (1935) Evidences of vascular occlusion in multiple sclerosis and encephalomyelitis. Arch Neuropsychol 32:1298–1321Google Scholar
  12. 12.
    Adams CW, Poston RN, Buk SJ, Sidhu YS, Vipond H (1985) Inflammatory vasculitis in multiple sclerosis. J Neurol Sci 69:269–283PubMedCrossRefGoogle Scholar
  13. 13.
    Adams CW (1988) Perivascular iron deposition and other vascular damage in multiple sclerosis. J Neurol Neurosurg Psychiatry 51:260–265PubMedCrossRefGoogle Scholar
  14. 14.
    Law M, Saindane AM, Ge Y et al (2004) Microvascular abnormality in relapsing-remitting multiple sclerosis: perfusion MR imaging findings in normal-appearing white matter. Radiology 231:645–652PubMedCrossRefGoogle Scholar
  15. 15.
    Zamboni P, Galeotti R, Menegatti E et al (2009) Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 80:392–399PubMedCrossRefGoogle Scholar
  16. 16.
    Hojnacki D, Zamboni P, Lopez-Soriano A et al (2010) Use of neck magnetic resonance venography, Doppler sonography and selective venography for diagnosis of chronic cerebrospinal venous insufficiency: a pilot study in multiple sclerosis patients and healthy controls. Int Angiol 29:127–139PubMedGoogle Scholar
  17. 17.
    Zamboni P, Galeotti R (2010) The chronic cerebrospinal venous insufficiency syndrome. Phlebology 25:269–279PubMedCrossRefGoogle Scholar
  18. 18.
    Ge Y, Zohrabian VM, Osa EO et al (2009) Diminished visibility of cerebral venous vasculature in multiple sclerosis by susceptibility-weighted imaging at 3.0 Tesla. J Magn Reson Imaging 29:1190–1194PubMedCrossRefGoogle Scholar
  19. 19.
    Boeckh-Behrens T, Lutz J, Lummel N et al (2011) Susceptibility-weighted angiography (SWAN) of cerebral veins and arteries compared to TOF-MRA. Eur J Radiol 81:1238–1245Google Scholar
  20. 20.
    Polman CH, Reingold SC, Banwell B et al (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69:292–302PubMedCrossRefGoogle Scholar
  21. 21.
    Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33:1444–1452PubMedCrossRefGoogle Scholar
  22. 22.
    Haacke EM, Xu Y, Cheng YC, Reichenbach JR (2004) Susceptibility weighted imaging (SWI). Magn Reson Med 52:612–618PubMedCrossRefGoogle Scholar
  23. 23.
    Tallantyre EC, Brookes MJ, Dixon JE, Morgan PS, Evangelou N, Morris PG (2008) Demonstrating the perivascular distribution of MS lesions in vivo with 7-Tesla MRI. Neurology 70:2076–2078PubMedCrossRefGoogle Scholar
  24. 24.
    Hammond KE, Metcalf M, Carvajal L et al (2008) Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron. Ann Neurol 64:707–713PubMedCrossRefGoogle Scholar
  25. 25.
    Varga AW, Johnson G, Babb JS et al (2009) White matter hemodynamic abnormalities precede sub-cortical gray matter changes in multiple sclerosis. J Neurol Sci 282:28–33PubMedCrossRefGoogle Scholar
  26. 26.
    Ge Y, Law M, Johnson G et al (2005) Dynamic susceptibility contrast perfusion MR imaging of multiple sclerosis: characterizing hemodynamic impairment and inflammatory activity. AJNR Am J Neuroradiol 26:1539–1547PubMedGoogle Scholar
  27. 27.
    Adhya S, Johnson G, Herbert J et al (2006) Pattern of hemodynamic impairment in multiple sclerosis: dynamic susceptibility contrast perfusion MR imaging at 3.0 T. Neuroimage 33:1029–1035PubMedCrossRefGoogle Scholar
  28. 28.
    Inglese M, Adhya S, Johnson G et al (2008) Perfusion magnetic resonance imaging correlates of neuropsychological impairment in multiple sclerosis. J Cereb Blood Flow Metab 28:164–171PubMedCrossRefGoogle Scholar
  29. 29.
    D’haeseleer M, Cambron M, Vanopdenbosch L, De Keyser J (2011) Vascular aspects of multiple sclerosis. Lancet Neurol 10:657–666PubMedCrossRefGoogle Scholar
  30. 30.
    Minagar A, Jy W, Jimenez JJ et al (2011) Elevated plasma endothelial microparticles in multiple sclerosis. Neurology 56:1319–1324CrossRefGoogle Scholar
  31. 31.
    Aksungar FB, Topkaya AE, Yildiz Z, Sahin S, Turk U (2008) Coagulation status and biochemical and inflammatory markers in multiple sclerosis. J Clin Neurosci 15:393–397PubMedCrossRefGoogle Scholar
  32. 32.
    Sheremata WA, Jy W, Horstman LL, Ahn YS, Alexander JS, Minagar A (2008) Evidence of platelet activation in multiple sclerosis. J Neuroinflammation 5:27PubMedCrossRefGoogle Scholar
  33. 33.
    Wakefield AJ, More LJ, Difford J, McLaughlin JE (1994) Immunohistochemical study of vascular injury in acute multiple sclerosis. J Clin Pathol 47:129–133PubMedCrossRefGoogle Scholar
  34. 34.
    Zamboni P, Menegatti E, Weinstock-Guttman B et al (2009) The severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis is related to altered cerebrospinal fluid dynamics. Funct Neurol 24:133–138PubMedGoogle Scholar
  35. 35.
    Zamboni P, Menegatti E, Weinstock-Guttman B et al (2011) Hypoperfusion of brain parenchyma is associated with the severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis: a cross-sectional preliminary report. BMC Med 9:22PubMedCrossRefGoogle Scholar
  36. 36.
    Kantarci F, Albayram S, Demirci NO et al (2011) Chronic cerebrospinal venous insufficiency: does ultrasound really distinguish multiple sclerosis subjects from healthy controls? Eur Radiol 22:970–979PubMedCrossRefGoogle Scholar
  37. 37.
    Zivadinov R, Poloni GU, Marr K et al (2011) Decreased brain venous vasculature visibility on susceptibility-weighted imaging venography in patients with multiple sclerosis is related to chronic cerebrospinal venous insufficiency. BMC Neurol 11:128PubMedCrossRefGoogle Scholar
  38. 38.
    Hochmeister S, Grundtner R, Bauer J et al (2006) Dysferlin is a new marker for leaky brain blood vessels in multiple sclerosis. J Neuropathol Exp Neurol 65:855–865PubMedCrossRefGoogle Scholar
  39. 39.
    Thompson AJ, Polman CH, Miller DH et al (1997) Primary progressive multiple sclerosis. Brain 120:1085–1096PubMedCrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2012

Authors and Affiliations

  • Chun Zeng
    • 1
  • Xuan Chen
    • 1
  • Yongmei Li
    • 1
  • Yu Ouyang
    • 1
  • Fajin Lv
    • 1
  • Reshiana Rumzan
    • 1
  • Zhongping Wang
    • 1
  1. 1.Department of Radiologythe First Affiliated Hospital of Chongqing Medical UniversityChongqingChina

Personalised recommendations