Patients with Multiple Sclerosis with Structural Venous Abnormalities on MR Imaging Exhibit an Abnormal Flow Distribution of the Internal Jugular Veins



      To evaluate extracranial venous structural and flow characteristics in patients with multiple sclerosis (MS).

      Materials and Methods

      Two hundred subjects with MS from two sites (n = 100 each) were evaluated with magnetic resonance (MR) imaging at 3 T. Contrast-enhanced time-resolved MR angiography and time-of-flight MR venography were used to assess vascular anatomy. Two-dimensional phase-contrast MR imaging was used to quantify blood flow. The MS population was divided into two groups: those with evident internal jugular vein (IJV) stenoses (stenotic group) and those without (nonstenotic group).


      Of the 200 patients, 136 (68%) showed IJV structural abnormalities, including unilateral or bilateral stenoses at different levels in the neck (n = 101; 50.5%) and atresia (n = 35; 17.5%). The total IJV flow normalized to the total arterial flow of the stenotic group (56% ± 22) was significantly lower than that of the nonstenotic group (77% ± 14; P < .001). The arterial/venous flow mismatch in the stenotic group (12% ± 15) was significantly greater than that in the nonstenotic group (6% ± 12; P < .001). The ratio of subdominant venous flow rate (Fsd) to dominant venous flow rate (Fd) for the stenotic group (0.38 ± 0.27) was significantly lower than for the nonstenotic group (0.59 ± 0.23; P < .001). The majority of the stenotic group (67%) also had an Fsd of less than 3 mL/s, a Fd/Fsd ratio greater than 3:1, and/or a total IJV flow rate of less than 8 mL/s.


      MR imaging provides a noninvasive means to separate stenotic from nonstenotic MS cases. The former group was more prevalent in the present MS population and carried significantly less flow in the IJVs than the latter.


      CCA (common carotid artery), CCSVI (chronic cerebrospinal venous insufficiency), CE (contrast-enhanced), EJV (external jugular vein), Fd (dominant venous flow rate), Fsd (subdominant venous flow rate), FIJV (IJV flow), Fta (total arterial flow), LIJV (left internal jugular vein), IJV (internal jugular vein), MIP (maximum-intensity projection), MS (multiple sclerosis), PC (phase-contrast), RIJV (right internal jugular vein), 3D (three-dimensional), TOF (time of flight), 2D (two-dimensional), Venc (encoding velocity)
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        • Zamboni P.
        • Galeotti R.
        • Menegatti E.
        • et al.
        Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis.
        J Neurol Neurosurg Psychiatry. 2009; 80: 392-399
        • Singh A.V.
        • Zamboni P.
        Anomalous venous blood flow and iron deposition in multiple sclerosis.
        J Cereb Blood Flow Metab. 2009; 29: 1867-1878
        • Zamboni P.
        • Galeotti R.
        • Menegatti E.
        • et al.
        A prospective open-label study of endovascular treatment of chronic cerebrospinal venous insufficiency.
        J Vasc Surg. 2009; 50: 1348-1358
        • Zamboni P.
        • Menegatti E.
        • Galeotti R.
        • et al.
        The value of cerebral Doppler venous haemodynamics in the assessment of multiple sclerosis.
        J Neurol Sci. 2009; 282: 21-27
        • Zamboni P.
        • Menegatti E.
        • Weinstock-Guttman B.
        • et al.
        The severity of chronic cerebrospinal venous insufficiency in patients with multiple sclerosis is related to altered cerebrospinal fluid dynamics.
        Funct Neurol. 2009; 24: 133-138
        • Doepp F.
        • Schreiber S.J.
        • von Münster T.
        • Rademacher J.
        • Klingebiel R.
        • Valdueza J.M.
        How does the blood leave the brain?.
        Neuroradiology. 2004; 46: 565-570
        • Doepp F.
        • Paul F.
        • Valdueza J.M.
        • Schmierer K.
        • Schreiber S.J.
        No cerebrocervical venous congestion in patients with multiple sclerosis.
        Ann Neurol. 2010; 68: 173-183
        • Chung C.P.
        • Lin Y.J.
        • Chao A.C.
        • et al.
        Jugular venous hemodynamic changes with aging.
        Ultras Med Biol. 2010; 36: 1776-1782
        • Sundström P.
        • Wåhlin A.
        • Ambarki K.
        • Birgander R.
        • Eklund A.
        • Malm J.
        Venous and cerebrospinal fluid flow in multiple sclerosis: a case-control study.
        Ann Neurol. 2010; 68: 255-259
        • Stoquart-Elsankari S.
        • Lehmann P.
        • Villette A.
        • et al.
        A phase-contrast MRI study of physiologic cerebral venous flow.
        J Cereb Blood Flow Metabol. 2009; 29: 1208-1215
        • Zivadinov R.
        • Galeotti R.
        • Hojnacki D.
        • et al.
        Value of MR venography for detection of internal jugular vein anomalies in multiple sclerosis: a pilot longitudinal study.
        AJNR Am J Neuroradiol. 2011; 32: 938-946
        • Zivadinov R.
        • Lopez-Soriano A.
        • Weinstock-Guttman B.
        • et al.
        Use of MR venography for characterization of the extracranial venous system in patients with multiple sclerosis and healthy control subjects.
        Radiology. 2011; 258: 562-570
        • Furukawa S.
        • Nakagawa T.
        • Sakaguchi I.
        • Nishi K.
        The diameter of the internal jugular vein studied by autopsy.
        Rom J Leg Med. 2010; 18: 125-128
        • Tartiere D.
        • Seguin P.
        • Juhel C.
        • Laviolle B.
        • Malledant Y.
        Estimation of the diameter and cross-sectional area of the internal jugular veins in adult patients.
        Crit Care. 2009; 13: R197
        • Montgomery D.C.
        Design and analysis of experiments.
        5th edition. Wiley, New York2000
        • Seoane E.
        • Rhoton Jr., A.L.
        Compression of the internal jugular vein by the transverse process of the atlas as the cause of cerebellar hemorrhage after supratentorial craniotomy.
        Surg Neurol. 1999; 51: 500-505
        • Khan O.
        • Filippi M.
        • Freedman M.S.
        • et al.
        Chronic cerebrospinal venous insufficiency and multiple sclerosis.
        Ann Neurol. 2010; 67: 286-290
        • Siskin G.P.
        • Haskal Z.J.
        • McLennan G.
        • et al.
        Development of a research agenda for evaluation of interventional therapies for chronic cerebrospinal venous insufficiency: proceedings from a multidisciplinary research consensus panel.
        J Vasc Interv Radiol. 2011; 22: 587-593
        • Zaharchuk G.
        • Fischbein N.J.
        • Rosenberg J.
        • Herfkens R.J.
        • Dake M.D.
        Comparison of MR and contrast venography of the cervical venous system in multiple sclerosis.
        AJNR Am J Neuroradiol. 2011; 32: 1482-1489
        • Chung C.P.
        • Hsu H.Y.
        • Chao A.C.
        • Sheng W.Y.
        • Soong B.W.
        • Hu H.H.
        Transient global amnesia: cerebral venous outflow impairment--insight from the abnormal flow patterns of the internal jugular vein.
        Ultras Med Biol. 2007; 33: 1727-1735
        • Hsu H.Y.
        • Chao A.C.
        • Chen Y.Y.
        • et al.
        Reflux of jugular and retrobulbar venous flow in transient monocular blindness.
        Ann Neurol. 2008; 63: 247-253
        • Zivadinov R.
        • Marr K.
        • Cutter G.
        • et al.
        Prevalence, sensitivity, and specificity of chronic cerebrospinal venous insufficiency in MS.
        Neurology. 2011; 77: 138-144