Mid-term sustained relief from headaches after balloon angioplasty of the internal jugular veins in patients with multiple sclerosis

Clive B Beggs, Alessia Giaquinta, Massimiliano Veroux, Ester De Marco, Dovile Mociskyte, Pierfrancesco Veroux, Clive B Beggs, Alessia Giaquinta, Massimiliano Veroux, Ester De Marco, Dovile Mociskyte, Pierfrancesco Veroux

Abstract

Objectives: Multiple sclerosis (MS) patients frequently suffer from headaches and fatigue, and many reports have linked headaches with intracranial and/or extracranial venous obstruction. We therefore designed a study involving MS patients diagnosed with obstructive disease of internal jugular veins (IJVs), with the aim of evaluating the impact of percutaneous transluminal angioplasty (PTA) on headache and fatigue indicators.

Methods: 286 MS patients (175 relapsing remitting (RR), 75 secondary progressive (SP), and 36 primary progressive (PP)), diagnosed with obstructive disease of IJVs, underwent PTA of IJVs during the period 2011-2015. This included 113 headache positive patients (82 RR, 22 SP, and 9 PP) and 277 fatigue positive patients (167 RR, 74 SP, and 36 PP). Migraine Disability Assessment (MIDAS), and the Fatigue Severity Scale (FSS) were evaluated: before PTA; 3-months after PTA; and at final follow-up in 2017. Patients were evaluated with Doppler sonography of the IJVs at 1, 6 and 12 months after PTA and yearly thereafter. Non-parametric statistical analysis was performed using a combination of the Friedman test and Spearman correlation analysis.

Results: With the exception of the PP patients there were significant reductions (all p < 0.001) in the MIDAS and FSS scores in the 3-month following PTA. The improvement in MIDAS score following PTA was maintained throughout the follow-up period in both the RR (p < 0.001; mean of 3.55 years) and SP (p = 0.002; mean of 3.52 years) MS cohorts. With FSS, significant improvement was only observed at 2017 follow-up in the RR patients (p < 0.001; mean of 3.37 years). In the headache-positive patients, post-PTA MIDAS score was significantly negatively correlated with the change in the blood flow score in the left (r = -0.238, p = 0.031) and right (r = -0.250, p = 0.023) IJVs in the RR patients and left IJV (r = -0.727, p = 0.026) in the PP patients. In the fatigue-positive cohort, post-PTA FSS score was also significantly negatively correlated with the change in blood flow in the right IJV in the PP patients (r = -0.423, p = 0.010). In addition, the pre and post-PTA FSS scores were significantly positively correlated in the fatigue-positive RR (r = 0.249, p = 0.001) and SP patients (r = 0.272, p = 0.019).

Conclusions: The intervention of PTA was associated with a large and sustained (>3 years) reduction in MIDAS score in both RR and SP MS patients. While a similar initial post-PTA reduction in FSS score was also observed, this was not maintained in the SP and PP patients, although it remained significant at follow-up (>3 years) in the RR MS patients. This suggests that venoplasty might be a useful intervention for treating patients with persistent headaches and selected concomitant obstructive disease of the IJVs.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1
MIDAS scores at pre-PTA, 3 months after PTA and final follow-up for the: (A) relapsing remitting (n = 82); (B) secondary progressive (n = 22); and (C) primary progressive (n = 9) multiple sclerosis patients.
Fig 2
Fig 2
FSS scores at pre-PTA, 3 months after PTA and final follow-up for the: (A) relapsing remitting (n = 167); (B) secondary progressive (n = 74); and (C) primary progressive (n = 26) multiple sclerosis patients.

References

    1. Simka M, Kostecki J, Zaniewski M, Majewski E, Hartel M. Extracranial Doppler sonographic criteria of chronic cerebrospinal venous insufficiency in the patients with multiple sclerosis. Int Angiol. 2010;29(2):109–14. .
    1. Zamboni P, Galeotti R, Menegatti E, Malagoni AM, Tacconi G, Dall'Ara S, et al. Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry. 2009;80(4):392–9. doi: .
    1. Zaniewski M, Kostecki J, Kuczmik W, Ziaja D, Opala G, Swiat M, et al. Neck duplex Doppler ultrasound evaluation for assessing chronic cerebrospinal venous insufficiency in multiple sclerosis patients. Phlebology. 2013;28(1):24–31. doi: .
    1. Zamboni P, Menegatti E, Conforti P, Shepherd S, Tessari M, Beggs C. Assessment of cerebral venous return by a novel plethysmography method. J Vasc Surg. 2012;56(3):677–85 e1. doi: .
    1. Haacke EM, Feng W, Utriainen D, Trifan G, Wu Z, Latif Z, et al. Patients with multiple sclerosis with structural venous abnormalities on MR imaging exhibit an abnormal flow distribution of the internal jugular veins. J Vasc Interv Radiol. 2012;23(1):60–8 e1-3. doi: .
    1. Petrov I, Grozdinski L, Kaninski G, Iliev N, Iloska M, Radev A. Safety profile of endovascular treatment for chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Endovasc Ther. 2011;18(3):314–23. doi: .
    1. Lupattelli T, Bellagamba G, Righi E, Di Donna V, Flaishman I, Fazioli R, et al. Feasibility and safety of endovascular treatment for chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Vasc Surg. 2013;58(6):1609–18. doi: .
    1. Radak D, Kolar J, Sagic D, Ilijevski N, Tanaskovic S, Aleksic N, et al. Percutaneous angioplasty of internal jugular and azygous veins in patients with chronic cerebrospinal venous insufficiency and multiple sclerosis: early and mid-term results. Phlebology. 2014;29(6):367–75. doi: .
    1. Mayer CA, Pfeilschifter W, Lorenz MW, Nedelmann M, Bechmann I, Steinmetz H, et al. The perfect crime? CCSVI not leaving a trace in MS. J Neurol Neurosurg Psychiatry. 2011;82(4):436–40. doi: .
    1. Mayer CA, Ziemann U. CCSVI: is blinding the key? Eur J Vasc Endovasc Surg. 2012;43(1):124–5. doi: .
    1. Zamboni P, Galeotti R, Menegatti E, Malagoni AM, Gianesini S, Bartolomei I, et al. A prospective open-label study of endovascular treatment of chronic cerebrospinal venous insufficiency. J Vasc Surg. 2009;50(6):1348–58 e1-3. doi: .
    1. Zamboni P, Galeotti R, Weinstock-Guttman B, Kennedy C, Salvi F, Zivadinov R. Venous angioplasty in patients with multiple sclerosis: results of a pilot study. Eur J Vasc Endovasc Surg. 2012;43(1):116–22. doi: .
    1. Bavera PM. May symptoms of chronic cerebrospinal venous insufficiency be improved by venous angioplasty? An independent 4-year follow up on 366 cases. Veins & Lymphatics. 2015;4:5400.
    1. Kostecki J, Zaniewski M, Ziaja K, Urbanek T, Kuczmik W, Krzystanek E, et al. An endovascular treatment of Chronic Cerebro-Spinal Venous Insufficiency in multiple sclerosis patients—6 month follow-up results. Neuro Endocrinol Lett. 2011;32(4):557–62. .
    1. Kostecki J, Zaniewski M, Urbanek T, Korzeniowski T, Ziaja D, Sznapka M. The hemodynamics of blood flow through the internal jugular veins after CCSVI endovascular treatment and its impact on the quality of life in patients with Chronic Cerebrospinal Venous Insufficiency. Brain Disorders & Therapy. 2016;5:3.
    1. Malagoni AM, Galeotti R, Menegatti E, Manfredini F, Basaglia N, Salvi F, et al. Is chronic fatigue the symptom of venous insufficiency associated with multiple sclerosis? A longitudinal pilot study. Int Angiol. 2010;29(2):176–82. .
    1. Pereira L, Campos Costa E, Nunes T, Saraiva P, Ferreira J, Cruz P, et al. Dynamics of a haemodynamic headache: A case report and literature review of headache secondary to flow inversion of the internal jugular vein. Cephalalgia. 2016;36(14):1370–8. doi: .
    1. Ittyachen AM, Vijayan A, Kottam P, Jose A. Aches, pains and headache: an unusual combination of hypothyroidism, vitamin D deficiency, cervical radiculopathy and cortical vein sinus thrombosis. BMJ Case Rep. 2015;2015 doi: .
    1. Sparaco M, Feleppa M, Bigal ME. Cerebral Venous Thrombosis and Headache—A Case-Series. Headache. 2015;55(6):806–14. doi: .
    1. Kiritsi O, Noussios G, Tsitas K, Chouridis P, Lappas D, Natsis K. Anatomical variants of the emissary veins: unilateral aplasia of both the sigmoid sinus and the internal jugular vein and development of the petrosquamosal sinus. A rare case report. Folia Morphol (Warsz). 2011;70(4):305–8. .
    1. Wasay M, Kojan S, Dai AI, Bobustuc G, Sheikh Z. Headache in Cerebral Venous Thrombosis: incidence, pattern and location in 200 consecutive patients. J Headache Pain. 2010;11(2):137–9. doi: .
    1. Alberti A, Venti M, Biagini S. Headache and cerebral vein and sinus thrombosis. Front Neurol Neurosci. 2008;23:89–95. doi: .
    1. Veroux P, Giaquinta A, Perricone D, Lupo L, Gentile F, Virgilio C, et al. Internal jugular veins out flow in patients with multiple sclerosis:a catheter venography study. J Vasc Interv Radiol. 2013;24(12):1790–7. .
    1. Giaquinta A, Beggs CB, Veroux M, De Marco E, Sanzone A, Virgilio C, et al. Factors influencing the hemodynamic response to balloon angioplasty in the treatment of outflow anomalies of internal jugular veins. Journal of Vascular Surgery: Venous and Lymphatic Disorders. 2017;epub ahead of print.
    1. Stewart WF, Lipton RB, Dowson AJ, Sawyer J. Development and testing of the Migraine Disability Assessment (MIDAS) Questionnaire to assess headache-related disability. Neurology. 2001;56(6 Suppl 1):S20–8. .
    1. D'Amico D, Mosconi P, Genco S, Usai S, Prudenzano AM, Grazzi L, et al. The Migraine Disability Assessment (MIDAS) questionnaire: translation and reliability of the Italian version. Cephalalgia. 2001;21(10):947–52. doi: .
    1. Hollander M, Wolfe DA. Nonparametric Statistical Methods. New York: J. Wiley; 1999.
    1. D'Amico D, Grazzi L, Usai S, Leonardi M, Raggi A. Disability and quality of life in headache: where we are now and where we are heading. Neurol Sci. 2013;34 Suppl 1:S1–5. doi: .
    1. Burch RC, Loder S, Loder E, Smitherman TA. The prevalence and burden of migraine and severe headache in the United States: updated statistics from government health surveillance studies. Headache. 2015;55(1):21–34. doi: .
    1. Silberstein SD, Dodick DW, Aurora SK, Diener HC, DeGryse RE, Lipton RB, et al. Per cent of patients with chronic migraine who responded per onabotulinumtoxinA treatment cycle: PREEMPT. J Neurol Neurosurg Psychiatry. 2015;86(9):996–1001. doi: .
    1. Day MA, Thorn BE, Rubin NJ. Mindfulness-based cognitive therapy for the treatment of headache pain: A mixed-methods analysis comparing treatment responders and treatment non-responders. Complement Ther Med. 2014;22(2):278–85. doi: .
    1. Chou CH, Chao AC, Lu SR, Hu HH, Wang SJ. Cephalic venous congestion aggravates only migraine-type headaches. Cephalalgia. 2004;24(11):973–9. doi: .
    1. Doepp F, Schreiber SJ, Dreier JP, Einhaupl KM, Valdueza JM. Migraine aggravation caused by cephalic venous congestion. Headache. 2003;43(2):96–8. .
    1. Chung CP, Chao AC, Hsu HY, Lin SJ, Hu HH. Decreased jugular venous distensibility in migraine. Ultrasound Med Biol. 2010;36(1):11–6. doi: .
    1. Kitano M, Oldendorf WH, Cassen B. The Elasticity of the Cranial Blood Pool. J Nucl Med. 1964;5:613–25. .
    1. Beggs CB. Venous hemodynamics in neurological disorders: an analytical review with hydrodynamic analysis. BMC Med. 2013;11:142 doi: .
    1. Gadda G, Taibi A, Sisini F, Gambaccini M, Zamboni P, Ursino M. A new hemodynamic model for the study of cerebral venous outflow. Am J Physiol Heart Circ Physiol. 2015;308(3):H217–31. doi: .
    1. Tessari M, Ciorba A, Mueller LO, Zhang Q, Cristini M, Menegatti E, et al. Jugular valve function and petrosal sinuses pressure: a computational model applied to sudden sensorineural hearing loss. Veins & Lymphatics. 2017;6:2.
    1. Beggs C, Shepherd S, Zamboni P. Cerebral venous outflow resistance and interpretation of cervical plethysmography data with respect to the diagnosis of chronic cerebrospinal venous insufficiency. Phlebology. 2014;29(3):191–99. doi: .
    1. Bateman GA, Lechner-Scott J, Lea RA. A comparison between the pathophysiology of multiple sclerosis and normal pressure hydrocephalus: is pulse wave encephalopathy a component of MS? Fluids Barriers CNS. 2016;13(1):18 doi: .
    1. Bateman GA, Lechner-Scott J, Copping R, Moeskops C, Yap SL. Comparison of the sagittal sinus cross-sectional area between patients with multiple sclerosis, hydrocephalus, intracranial hypertension and spontaneous intracranial hypotension: a surrogate marker of venous transmural pressure? Fluids Barriers CNS. 2017;14(1):18 doi: .
    1. Lagana MM, Shepherd SJ, Cecconi P, Beggs CB. Intracranial volumetric changes govern cerebrospinal fluid flow in the Aqueduct of Sylvius in healthy adults. Biomedical Signal Processing and Control. 2017;36:84–92.
    1. Bateman GA. Vascular compliance in normal pressure hydrocephalus. AJNR Am J Neuroradiol. 2000;21(9):1574–85. .
    1. Bateman GA. The pathophysiology of idiopathic normal pressure hydrocephalus: cerebral ischemia or altered venous hemodynamics? AJNR Am J Neuroradiol. 2008;29(1):198–203. doi: .
    1. Hatt A, Cheng S, Tan K, Sinkus R, Bilston LE. MR Elastography Can Be Used to Measure Brain Stiffness Changes as a Result of Altered Cranial Venous Drainage During Jugular Compression. AJNR Am J Neuroradiol. 2015;36(10):1971–7. doi: .
    1. Watkins SM, Espir M. Migraine and multiple sclerosis. J Neurol Neurosurg Psychiatry. 1969;32(1):35–7. .
    1. Kister I, Caminero AB, Monteith TS, Soliman A, Bacon TE, Bacon JH, et al. Migraine is comorbid with multiple sclerosis and associated with a more symptomatic MS course. J Headache Pain. 2010;11(5):417–25. doi: .
    1. Adhya S, Johnson G, Herbert J, Jaggi H, Babb JS, Grossman RI, et al. Pattern of hemodynamic impairment in multiple sclerosis: dynamic susceptibility contrast perfusion MR imaging at 3.0 T. Neuroimage. 2006;33(4):1029–35. doi: .
    1. Ge Y, Law M, Johnson G, Herbert J, Babb JS, Mannon LJ, et al. Dynamic susceptibility contrast perfusion MR imaging of multiple sclerosis lesions: characterizing hemodynamic impairment and inflammatory activity. AJNR Am J Neuroradiol. 2005;26(6):1539–47. .
    1. Varga AW, Johnson G, Babb JS, Herbert J, Grossman RI, Inglese M. White matter hemodynamic abnormalities precede sub-cortical gray matter changes in multiple sclerosis. J Neurol Sci. 2009;282(1–2):28–33. doi: .
    1. Holland CM, Charil A, Csapo I, Liptak Z, Ichise M, Khoury SJ, et al. The relationship between normal cerebral perfusion patterns and white matter lesion distribution in 1,249 patients with multiple sclerosis. J Neuroimaging. 2012;22(2):129–36. doi: .
    1. Denuelle M, Fabre N, Payoux P, Chollet F, Geraud G. Posterior cerebral hypoperfusion in migraine without aura. Cephalalgia. 2008;28(8):856–62. doi: .
    1. Olesen J, Larsen B, Lauritzen M. Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol. 1981;9(4):344–52. doi: .
    1. Vijayan N. Spreading cerebral hypoperfusion during migraine headache. N Engl J Med. 1995;332(22):1516 doi: .
    1. Lange G, Holodny AI, DeLuca J, Lee HJ, Yan XH, Steffener J, et al. Quantitative assessment of cerebral ventricular volumes in chronic fatigue syndrome. Appl Neuropsychol. 2001;8(1):23–30. doi: .
    1. Sander C, Eling P, Hanken K, Klein J, Kastrup A, Hildebrandt H. The Impact of MS-Related Cognitive Fatigue on Future Brain Parenchymal Loss and Relapse: A 17-Month Follow-up Study. Front Neurol. 2016;7:155 doi: .
    1. Zamboni P, Menegatti E, Weinstock-Guttman B, Schirda C, Cox JL, Malagoni AM, 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(3):133–8. .
    1. Gorucu Y, Albayram S, Balci B, Hasiloglu ZI, Yenigul K, Yargic F, et al. Cerebrospinal fluid flow dynamics in patients with multiple sclerosis: a phase contrast magnetic resonance study. Funct Neurol. 2011;26(4):215–22. .
    1. Beggs CB, Magnano C, Shepherd SJ, Marr K, Valnarov V, Hojnacki D, et al. Aqueductal cerebrospinal fluid pulsatility in healthy individuals is affected by impaired cerebral venous outflow. J Magn Reson Imaging. 2014;40(5):1215–22. doi: .
    1. Zivadinov R, Magnano C, Galeotti R, Schirda C, Menegatti E, Weinstock-Guttman B, et al. Changes of cine cerebrospinal fluid dynamics in patients with multiple sclerosis treated with percutaneous transluminal angioplasty: a case-control study. J Vasc Interv Radiol. 2013;24(6):829–38. doi: .
    1. Zamboni P, Menegatti E, Cittanti C, Sisini F, Gianesini S, Salvi F, et al. Fixing the jugular flow reduces ventricle volume and improves brain perfusion. J Vasc Surg Venous Lymphat Disord. 2016;4(4):434–45. doi: .

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