Internal jugular vein insufficiency syndrome_West China Medical Journal

Authors：

YANG Xiaoyan ^1,2 , YAN Feng ³ , MENG Ran ^1,4 , ZHOU Bing ² ,  JI Xunming ^1,3

1. Department of China-America Institute of Neuroscience, Xuanwu Hospital, Capital Medical University, Beijing 100053, P. R. China;
2. Beijing Advanced Innovation Center for Big Data-Based Precision Medicine, Beihang University, Beijing 100083, P. R. China;
3. Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, Beijing 100053, P. R. China;
4. Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing 100053, P. R. China;

Corresponding author：

JI Xunming, Email: jixm@ccmu.edu.cn

Keywords：

Internal jugular vein stenosis; Jugular venous reflux; Cerebral ischemia; Etiology; Clinical symptoms

DOI：

10.7507/1002-0179.201806054

Video：

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Abstract Full text Figures/Tables Video References Cited by

Long-term chronic internal jugular vein (IJV) insufficiency, originally viewed as a non-pathological finding, may result in cerebral venous outflow disturbance, leading to cerebral venous ischemia and cerebral nervous functional disorders. In this article we discuss probable etiologies, symptoms, diagnosis and treatment of IJV disturbance, so as to provide some insights for clinicians.

Citation： YANG Xiaoyan, YAN Feng, MENG Ran, ZHOU Bing, JI Xunming. Internal jugular vein insufficiency syndrome. West China Medical Journal, 2018, 33(6): 644-650. doi: 10.7507/1002-0179.201806054 Copy

1.	Torres C, Hogan M, Patro S, et al. Extracranial venous abnormalities: a true pathological finding in patients with multiple sclerosis or an anatomical variant? Eur Radiol, 2017, 27(1): 239-246.
2.	Buch K, Groller R, Nadgir RN, et al. Variability in the Cross-Sectional area and narrowing of the internal jugular vein in patients without multiple sclerosis. AJR Am J Roentgenol, 2016, 206(5): 1082-1086.
3.	Zamboni P, Galeotti R, Menegatti E, et al. Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry, 2009, 80(4): 392-399.
4.	Zivadinov R, Chung CP. Potential involvement of the extracranial venous system in central nervous system disorders and aging. BMC Med, 2013, 11: 260.
5.	Toro EF. Brain venous haemodynamics, neurological diseases and mathematical modelling. A review. Appl Math Comput, 2016, 272: 542-579.
6.	Zamboni P, Tesio L, Galimberti S, et al. Efficacy and safety of extracranial vein angioplasty in multiple sclerosis: a randomized clinical trial. JAMA Neurol, 2018, 75(1): 35-43.
7.	Traboulsee AL, Knox KB, Machan L, et al. Prevalence of extracranial venous narrowing on catheter venography in people with multiple sclerosis, their siblings, and unrelated healthy controls: a blinded, case-control study. Lancet, 2014, 383(9912): 138-145.
8.	Simka M. Chronic cerebrospinal venous insufficiency current perspectives. J Vasc Diag, 2014, 2: 1-13.
9.	Zivadinov R, Weinstock-Guttman B. Role of venoplasty for treatment of multiple sclerosis: value of open-label studies and surrogate treatment outcomes. J Vasc Interv Radiol, 2012, 23(10): 1308-1310.
10.	Beggs CB. The venous connection: the role of veins in neurodegenerative disease//Minagar A, AlexanderJ. Inflammatory disorders of the nervous system: pathogenesis, immunology, and clinical management. Clifton: Humana Press, 2017: 259-273.
11.	Beggs CB, Magnano C, Shepherd SJ, et al. Aqueductal cerebrospinal fluid pulsatility in healthy individuals is affected by impaired cerebral venous outflow. J Magn Reson Imaging, 2014, 40(5): 1215-1222.
12.	Zivadinov R, Magnano C, Galeotti R, 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): 829-838.
13.	Müller LO, Toro EF, Haacke EM, et al. Impact of CCSVI on cerebral haemodynamics: a mathematical study using MRI angiographic and flow data. Phlebology, 2016, 31(5): 305-324.
14.	Beggs CB. Venous hemodynamics in neurological disorders: an analytical review with hydrodynamic analysis. BMC Med, 2013, 11: 142.
15.	Hatt A, Cheng S, Tan K, et al. 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): 1971-1977.
16.	Chung CP, Wang PN, Wu YH, et al. More severe white matter changes in the elderly with jugular venous reflux. Ann Neurol, 2011, 69(3): 553-559.
17.	Chung CP, Hsu HY, Chao AC, et al. Jugular venous reflux affects ocular venous system in transient monocular blindness. Cerebrovasc Dis, 2010, 29(2): 122-129.
18.	Dolic K, Zivadinov R. The role of diagnostic imaging techniques for detection of extracranial venous system abnormalities associated// Saba L, Raz E. Neurovascular Imaging. New York: Springer, 2016: 1-30.
19.	Doepp F, Schreiber SJ, von Münster T, et al. How does the blood leave the brain? A systematic ultrasound analysis of cerebral venous drainage patterns. Neuroradiology, 2004, 46(7): 565-570.
20.	Dolic K, Marr K, Valnarov V, et al. Intra- and extraluminal structural and functional venous anomalies in multiple sclerosis, as evidenced by 2 noninvasive imaging techniques. AJNR Am J Neuroradiol, 2012, 33(1): 16-23.
21.	Lee BB, Baumgartner I, Berlien P, et al. Diagnosis and treatment of venous malformations. Consensus Document of the International Union of Phlebology (IUP): updated 2013. Int Angiol, 2015, 34(2): 97-149.
22.	Lee AB, Laredo J, Neville R. Embryological background of truncular venous malformation in the extracranial venous pathways as the cause of chronic cerebro spinal venous insufficiency. Int Angiol, 2010, 29(2): 95-108.
23.	Dolic K, Weinstock-Guttman B, Marr K, et al. Risk factors for chronic cerebrospinal venous insufficiency (CCSVI) in a large cohort of volunteers. PLoS One, 2011, 6(11): e28062.
24.	Dolic K, Weinstock-Guttman B, Marr K, et al. Heart disease, overweight, and cigarette smoking are associated with increased prevalence of extra-cranial venous abnormalities. Neurol Res, 2012, 34(8): 819-827.
25.	Thibault P, Attia J, Oldmeadow C. A prolonged antibiotic protocol to treat persistent Chlamydophila pneumoniae infection improves the extracranial venous circulation in multiple sclerosis. Phlebology, 2018, 33(6): 397-406.
26.	Zamboni P, Tisato V, Menegatti E, et al. Ultrastructure of internal jugular vein defective valves. Phlebology, 2015, 30(9): 644-647.
27.	Laganà MM, Di Rienzo M, Rizzo F, et al. Cardiac, respiratory and postural influences on venous return of internal jugular and vertebral veins. Ultrasound Med Biol, 2017, 43(6): 1195-1204.
28.	Diaconu CI, Fox RJ, Grattan A, et al. Hydration status substantially affects chronic cerebrospinal venous insufficiency assessments. Neurol Clin Pract, 2013, 3(5): 386-391.
29.	Valdueza JM, von Münster T, Hoffman O, et al. Postural dependency of the cerebral venous outflow. Lancet, 2000, 355(9199): 200-201.
30.	Djordje R, Nenad I, Jovo K, et al. Incidence and distribution of extravascular compression of extracranial venous pathway in patients with chronic cerebrospinal venous insufficiency and multiple sclerosis. Phlebology, 2014, 29(7): 476-479.
31.	Gianesini S, Menegatti E, Mascoli F, et al. The omohyoid muscle entrapment of the internal jugular vein. A still unclear pathogenetic mechanism. Phlebology, 2014, 29(9): 632-635.
32.	Schaller B. Physiology of cerebral venous blood flow: from experimental data in animals to normal function in humans. Brain Res Brain Res Rev, 2004, 46(3): 243-260.
33.	Mandolesi S, d’Alessandro A, Niglio T, et al. Jugular diameter and venous reflux. Ann Ital Chir, 2016, 87: 129-137.
34.	Doepp F, Bähr D, John M, et al. Internal jugular vein valve incompetence in COPD and primary pulmonary hypertension. J Clin Ultrasound, 2008, 36(8): 480-484.
35.	Dresser LP, McKinney WM. Anatomic and pathophysiologic studies of the human internal jugular valve. Am J Surg, 1987, 154(2): 220-224.
36.	Nedelmann M, Eicke BM, Dieterich M. Functional and morphological criteria of internal jugular valve insufficiency as assessed by ultrasound. J Neuroimaging, 2005, 15(1): 70-75.
37.	Lewis SL. Aetiology of transient global amnesia. Lancet, 1998, 352(9125): 397-399.
38.	Chung CP, Hsu HY, Chao AC, et al. Detection of intracranial venous reflux in patients of transient global amnesia. Neurology, 2006, 66(12): 1873-1877.
39.	Chung CP, Lin YJ, Chao AC, et al. Jugular venous hemodynamic changes with aging. Ultrasound Med Biol, 2010, 36(11): 1776-1782.
40.	Menegatti E, Tessari M, Vannini ME, et al. High resolution M-Mode evaluation of jugular vein valves in patients with neurological and neurosensory disorders. Curr Neurovasc Res, 2017, 14(4): 316-322.
41.	Chung CP, Chao AC, Hsu HY, et al. Decreased jugular venous distensibility in migraine. Ultrasound Med Biol, 2010, 36(1): 11-16.
42.	Liu M, Xu H, Wang Y, et al. Patterns of chronic venous insufficiency in the dural sinuses and extracranial draining veins and their relationship with white matter hyperintensities for patients with Parkinson’s disease. J Vasc Surg, 2015, 61(6): 1511-1520.e1.
43.	Chung CP, Beggs C, Wang PN, et al. Jugular venous reflux and white matter abnormalities in Alzheimer’s disease: a pilot study. J Alzheimers Dis, 2014, 39(3): 601-609.
44.	Attanasio G, Cagnoni L, Masci E, et al. Chronic cerebrospinal venous insufficiency as a cause of inner ear diseases. Acta Otolaryngol, 2017, 137(5): 460-463.
45.	Doepp F, Valdueza JM, Schreiber SJ. Incompetence of internal jugular valve in patients with primary exertional headache: a risk factor?. Cephalalgia, 2008, 28(2): 182-185.
46.	Koerte IK, Schankin CJ, Immler S, et al. Altered cerebrovenous drainage in patients with migraine as assessed by phase-contrast magnetic resonance imaging. Invest Radiol, 2011, 46(7): 434-440.
47.	Bruno A, Napolitano M, Califano L, et al. The prevalence of chronic cerebrospinal venous insufficiency in meniere disease: 24-month follow-up after angioplasty. J Vasc Interv Radiol, 2017, 28(3): 388-391.
48.	Di Berardino F, Alpini DC, Bavera PM, et al. Chronic cerebrospinal venous insufficiency in Meniere disease. Phlebology, 2015, 30(4): 274-279.
49.	Piraino D, Andolina G, Messina A. Truncular venous malformations in menière disease patients: the key for a new treatment perspective?. J Vasc Interv Radiol, 2016, 27(5): 766-768.e1.
50.	Bruno A, Califano L, Mastrangelo D, et al. Chronic cerebrospinal venous insufficiency in Méniere’s disease: diagnosis and treatment. Veins Lymphatics, 2014, 3(3854): 77-80.
51.	Merchant SN, Adams JC, Nadol JB. Pathophysiology of Meniere’s syndrome: are symptoms caused by endolymphatic hydrops?. Otol Neurotol, 2005, 26(1): 74-81.
52.	Akkawi NM, Agosti C, Rozzini L, et al. Transient global amnesia and disturbance of venous flow patterns. Lancet, 2001, 357(9260): 957.
53.	Chung CP, Hu HH. Pathogenesis of leukoaraiosis: role of jugular venous reflux. Med Hypotheses, 2010, 75(1): 85-90.
54.	Pantoni L, Garcia JH. Pathogenesis of leukoaraiosis: a review. Stroke, 1997, 28(3): 652-659.
55.	Cheng CY, Chang FC, Chao AC, et al. Internal jugular venous abnormalities in transient monocular blindness. BMC Neurol, 2013, 13: 94.
56.	Adamczyk-Ludyga A, Wróbel J, Simka M, et al. Retinal abnormalities in multiple sclerosis patients with associated chronic cerebrospinal venous insufficiency. Veins lymphatics, 2012, 1(e2): 1-6.
57.	Sternberg Z, Grewal P, Cen S, et al. Blood pressure normalization post-jugular venous balloon angioplasty. Phlebology, 2015, 30(4): 280-287.
58.	Ghezzi A, Annovazzi P, Amato MP, et al. Adverse events after endovascular treatment of chronic cerebro-spinal venous insufficiency (CCSVI) in patients with multiple sclerosis. Mult Scler, 2013, 19(7): 961-963.
59.	Hubbard D, Ponec D, Gooding J, et al. Clinical improvement after extracranial venoplasty in multiple sclerosis. J Vasc Interv Radiol, 2012, 23(10): 1302-1308.
60.	Zorc M, Denislic, M, Milosevic Z, et al. CRT-300.04. does an endovascular procedure improve the quality of life in patients with multiple sclerosis. JACC Cardiovasc Interv, 2016, 9(4 Suppl): S34.
61.	Folmer RL, Griest SE, Meikle MB, et al. Tinnitus severity, loudness, and depression. Otolaryngol Head Neck Surg, 1999, 121(1): 48-51.
62.	Wilson PH, Henry J, Bowen M, et al. Tinnitus reaction questionnaire: psychometric properties of a measure of distress associated with tinnitus. J Speech Hear Res, 1991, 34(1): 197-201.
63.	Hofmann E, Behr R, Neumann-Haefelin T, et al. Pulsatile tinnitus: imaging and differential diagnosis. Dtsch Arztebl Int, 2013, 110(26): 451-458.
64.	Liu H, Cao X, Zhang M, et al. A case report of cough headache with transient elevation of intracranial pressure and bilateral internal jugular vein valve incompetence: a primary or secondary headache?. Cephalalgia, 2018, 38(3): 600-603.
65.	Styczynski G, Dobosiewicz A, Abramczyk P, et al. Internal jugular vein valve insufficiency in cough syncope. Neurology, 2008, 70(10): 812-813.
66.	Zivadinov R, Bastianello S, Dake MD, et al. Recommendations for multimodal noninvasive and invasive screening for detection of extracranial venous abnormalities indicative of chronic cerebrospinal venous insufficiency: a position statement of the International Society for Neurovascular Disease. J Vasc Interv Radiol, 2014, 25(11): 1785-1794.e17.
67.	Caprio MG, Marr K, Gandhi S, et al. Centralized and local color doppler ultrasound reading agreement for diagnosis of the chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. Curr Neurovasc Res, 2017, 14(3): 266-273.
68.	Scalise F, Novelli E, Farina M, et al. Venous hemodynamic insufficiency severity score variation after endovascular treatment of chronic cerebrospinal venous insufficiency. Phlebology, 2015, 30(4): 250-256.
69.	Zamboni P, Menegatti E, Cittanti C, et al. Fixing the jugular flow reduces ventricle volume and improves brain perfusion. J Vasc Surg Venous Lymphat Disord, 2016, 4(4): 434-445.
70.	Sadovnick AD, Yee IM, Attwell-Pope K, et al. Patient-Reported benefits of extracranial venous therapy: British Columbia CCSVI registry. Can J Neurol Sci, 2017, 44(3): 246-254.

1. Torres C, Hogan M, Patro S, et al. Extracranial venous abnormalities: a true pathological finding in patients with multiple sclerosis or an anatomical variant? Eur Radiol, 2017, 27(1): 239-246.
2. Buch K, Groller R, Nadgir RN, et al. Variability in the Cross-Sectional area and narrowing of the internal jugular vein in patients without multiple sclerosis. AJR Am J Roentgenol, 2016, 206(5): 1082-1086.
3. Zamboni P, Galeotti R, Menegatti E, et al. Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry, 2009, 80(4): 392-399.
4. Zivadinov R, Chung CP. Potential involvement of the extracranial venous system in central nervous system disorders and aging. BMC Med, 2013, 11: 260.
5. Toro EF. Brain venous haemodynamics, neurological diseases and mathematical modelling. A review. Appl Math Comput, 2016, 272: 542-579.
6. Zamboni P, Tesio L, Galimberti S, et al. Efficacy and safety of extracranial vein angioplasty in multiple sclerosis: a randomized clinical trial. JAMA Neurol, 2018, 75(1): 35-43.
7. Traboulsee AL, Knox KB, Machan L, et al. Prevalence of extracranial venous narrowing on catheter venography in people with multiple sclerosis, their siblings, and unrelated healthy controls: a blinded, case-control study. Lancet, 2014, 383(9912): 138-145.
8. Simka M. Chronic cerebrospinal venous insufficiency current perspectives. J Vasc Diag, 2014, 2: 1-13.
9. Zivadinov R, Weinstock-Guttman B. Role of venoplasty for treatment of multiple sclerosis: value of open-label studies and surrogate treatment outcomes. J Vasc Interv Radiol, 2012, 23(10): 1308-1310.
10. Beggs CB. The venous connection: the role of veins in neurodegenerative disease//Minagar A, AlexanderJ. Inflammatory disorders of the nervous system: pathogenesis, immunology, and clinical management. Clifton: Humana Press, 2017: 259-273.
11. Beggs CB, Magnano C, Shepherd SJ, et al. Aqueductal cerebrospinal fluid pulsatility in healthy individuals is affected by impaired cerebral venous outflow. J Magn Reson Imaging, 2014, 40(5): 1215-1222.
12. Zivadinov R, Magnano C, Galeotti R, 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): 829-838.
13. Müller LO, Toro EF, Haacke EM, et al. Impact of CCSVI on cerebral haemodynamics: a mathematical study using MRI angiographic and flow data. Phlebology, 2016, 31(5): 305-324.
14. Beggs CB. Venous hemodynamics in neurological disorders: an analytical review with hydrodynamic analysis. BMC Med, 2013, 11: 142.
15. Hatt A, Cheng S, Tan K, et al. 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): 1971-1977.
16. Chung CP, Wang PN, Wu YH, et al. More severe white matter changes in the elderly with jugular venous reflux. Ann Neurol, 2011, 69(3): 553-559.
17. Chung CP, Hsu HY, Chao AC, et al. Jugular venous reflux affects ocular venous system in transient monocular blindness. Cerebrovasc Dis, 2010, 29(2): 122-129.
18. Dolic K, Zivadinov R. The role of diagnostic imaging techniques for detection of extracranial venous system abnormalities associated// Saba L, Raz E. Neurovascular Imaging. New York: Springer, 2016: 1-30.
19. Doepp F, Schreiber SJ, von Münster T, et al. How does the blood leave the brain? A systematic ultrasound analysis of cerebral venous drainage patterns. Neuroradiology, 2004, 46(7): 565-570.
20. Dolic K, Marr K, Valnarov V, et al. Intra- and extraluminal structural and functional venous anomalies in multiple sclerosis, as evidenced by 2 noninvasive imaging techniques. AJNR Am J Neuroradiol, 2012, 33(1): 16-23.
21. Lee BB, Baumgartner I, Berlien P, et al. Diagnosis and treatment of venous malformations. Consensus Document of the International Union of Phlebology (IUP): updated 2013. Int Angiol, 2015, 34(2): 97-149.
22. Lee AB, Laredo J, Neville R. Embryological background of truncular venous malformation in the extracranial venous pathways as the cause of chronic cerebro spinal venous insufficiency. Int Angiol, 2010, 29(2): 95-108.
23. Dolic K, Weinstock-Guttman B, Marr K, et al. Risk factors for chronic cerebrospinal venous insufficiency (CCSVI) in a large cohort of volunteers. PLoS One, 2011, 6(11): e28062.
24. Dolic K, Weinstock-Guttman B, Marr K, et al. Heart disease, overweight, and cigarette smoking are associated with increased prevalence of extra-cranial venous abnormalities. Neurol Res, 2012, 34(8): 819-827.
25. Thibault P, Attia J, Oldmeadow C. A prolonged antibiotic protocol to treat persistent Chlamydophila pneumoniae infection improves the extracranial venous circulation in multiple sclerosis. Phlebology, 2018, 33(6): 397-406.
26. Zamboni P, Tisato V, Menegatti E, et al. Ultrastructure of internal jugular vein defective valves. Phlebology, 2015, 30(9): 644-647.
27. Laganà MM, Di Rienzo M, Rizzo F, et al. Cardiac, respiratory and postural influences on venous return of internal jugular and vertebral veins. Ultrasound Med Biol, 2017, 43(6): 1195-1204.
28. Diaconu CI, Fox RJ, Grattan A, et al. Hydration status substantially affects chronic cerebrospinal venous insufficiency assessments. Neurol Clin Pract, 2013, 3(5): 386-391.
29. Valdueza JM, von Münster T, Hoffman O, et al. Postural dependency of the cerebral venous outflow. Lancet, 2000, 355(9199): 200-201.
30. Djordje R, Nenad I, Jovo K, et al. Incidence and distribution of extravascular compression of extracranial venous pathway in patients with chronic cerebrospinal venous insufficiency and multiple sclerosis. Phlebology, 2014, 29(7): 476-479.
31. Gianesini S, Menegatti E, Mascoli F, et al. The omohyoid muscle entrapment of the internal jugular vein. A still unclear pathogenetic mechanism. Phlebology, 2014, 29(9): 632-635.
32. Schaller B. Physiology of cerebral venous blood flow: from experimental data in animals to normal function in humans. Brain Res Brain Res Rev, 2004, 46(3): 243-260.
33. Mandolesi S, d’Alessandro A, Niglio T, et al. Jugular diameter and venous reflux. Ann Ital Chir, 2016, 87: 129-137.
34. Doepp F, Bähr D, John M, et al. Internal jugular vein valve incompetence in COPD and primary pulmonary hypertension. J Clin Ultrasound, 2008, 36(8): 480-484.
35. Dresser LP, McKinney WM. Anatomic and pathophysiologic studies of the human internal jugular valve. Am J Surg, 1987, 154(2): 220-224.
36. Nedelmann M, Eicke BM, Dieterich M. Functional and morphological criteria of internal jugular valve insufficiency as assessed by ultrasound. J Neuroimaging, 2005, 15(1): 70-75.
37. Lewis SL. Aetiology of transient global amnesia. Lancet, 1998, 352(9125): 397-399.
38. Chung CP, Hsu HY, Chao AC, et al. Detection of intracranial venous reflux in patients of transient global amnesia. Neurology, 2006, 66(12): 1873-1877.
39. Chung CP, Lin YJ, Chao AC, et al. Jugular venous hemodynamic changes with aging. Ultrasound Med Biol, 2010, 36(11): 1776-1782.
40. Menegatti E, Tessari M, Vannini ME, et al. High resolution M-Mode evaluation of jugular vein valves in patients with neurological and neurosensory disorders. Curr Neurovasc Res, 2017, 14(4): 316-322.
41. Chung CP, Chao AC, Hsu HY, et al. Decreased jugular venous distensibility in migraine. Ultrasound Med Biol, 2010, 36(1): 11-16.
42. Liu M, Xu H, Wang Y, et al. Patterns of chronic venous insufficiency in the dural sinuses and extracranial draining veins and their relationship with white matter hyperintensities for patients with Parkinson’s disease. J Vasc Surg, 2015, 61(6): 1511-1520.e1.
43. Chung CP, Beggs C, Wang PN, et al. Jugular venous reflux and white matter abnormalities in Alzheimer’s disease: a pilot study. J Alzheimers Dis, 2014, 39(3): 601-609.
44. Attanasio G, Cagnoni L, Masci E, et al. Chronic cerebrospinal venous insufficiency as a cause of inner ear diseases. Acta Otolaryngol, 2017, 137(5): 460-463.
45. Doepp F, Valdueza JM, Schreiber SJ. Incompetence of internal jugular valve in patients with primary exertional headache: a risk factor?. Cephalalgia, 2008, 28(2): 182-185.
46. Koerte IK, Schankin CJ, Immler S, et al. Altered cerebrovenous drainage in patients with migraine as assessed by phase-contrast magnetic resonance imaging. Invest Radiol, 2011, 46(7): 434-440.
47. Bruno A, Napolitano M, Califano L, et al. The prevalence of chronic cerebrospinal venous insufficiency in meniere disease: 24-month follow-up after angioplasty. J Vasc Interv Radiol, 2017, 28(3): 388-391.
48. Di Berardino F, Alpini DC, Bavera PM, et al. Chronic cerebrospinal venous insufficiency in Meniere disease. Phlebology, 2015, 30(4): 274-279.
49. Piraino D, Andolina G, Messina A. Truncular venous malformations in menière disease patients: the key for a new treatment perspective?. J Vasc Interv Radiol, 2016, 27(5): 766-768.e1.
50. Bruno A, Califano L, Mastrangelo D, et al. Chronic cerebrospinal venous insufficiency in Méniere’s disease: diagnosis and treatment. Veins Lymphatics, 2014, 3(3854): 77-80.
51. Merchant SN, Adams JC, Nadol JB. Pathophysiology of Meniere’s syndrome: are symptoms caused by endolymphatic hydrops?. Otol Neurotol, 2005, 26(1): 74-81.
52. Akkawi NM, Agosti C, Rozzini L, et al. Transient global amnesia and disturbance of venous flow patterns. Lancet, 2001, 357(9260): 957.
53. Chung CP, Hu HH. Pathogenesis of leukoaraiosis: role of jugular venous reflux. Med Hypotheses, 2010, 75(1): 85-90.
54. Pantoni L, Garcia JH. Pathogenesis of leukoaraiosis: a review. Stroke, 1997, 28(3): 652-659.
55. Cheng CY, Chang FC, Chao AC, et al. Internal jugular venous abnormalities in transient monocular blindness. BMC Neurol, 2013, 13: 94.
56. Adamczyk-Ludyga A, Wróbel J, Simka M, et al. Retinal abnormalities in multiple sclerosis patients with associated chronic cerebrospinal venous insufficiency. Veins lymphatics, 2012, 1(e2): 1-6.
57. Sternberg Z, Grewal P, Cen S, et al. Blood pressure normalization post-jugular venous balloon angioplasty. Phlebology, 2015, 30(4): 280-287.
58. Ghezzi A, Annovazzi P, Amato MP, et al. Adverse events after endovascular treatment of chronic cerebro-spinal venous insufficiency (CCSVI) in patients with multiple sclerosis. Mult Scler, 2013, 19(7): 961-963.
59. Hubbard D, Ponec D, Gooding J, et al. Clinical improvement after extracranial venoplasty in multiple sclerosis. J Vasc Interv Radiol, 2012, 23(10): 1302-1308.
60. Zorc M, Denislic, M, Milosevic Z, et al. CRT-300.04. does an endovascular procedure improve the quality of life in patients with multiple sclerosis. JACC Cardiovasc Interv, 2016, 9(4 Suppl): S34.
61. Folmer RL, Griest SE, Meikle MB, et al. Tinnitus severity, loudness, and depression. Otolaryngol Head Neck Surg, 1999, 121(1): 48-51.
62. Wilson PH, Henry J, Bowen M, et al. Tinnitus reaction questionnaire: psychometric properties of a measure of distress associated with tinnitus. J Speech Hear Res, 1991, 34(1): 197-201.
63. Hofmann E, Behr R, Neumann-Haefelin T, et al. Pulsatile tinnitus: imaging and differential diagnosis. Dtsch Arztebl Int, 2013, 110(26): 451-458.
64. Liu H, Cao X, Zhang M, et al. A case report of cough headache with transient elevation of intracranial pressure and bilateral internal jugular vein valve incompetence: a primary or secondary headache?. Cephalalgia, 2018, 38(3): 600-603.
65. Styczynski G, Dobosiewicz A, Abramczyk P, et al. Internal jugular vein valve insufficiency in cough syncope. Neurology, 2008, 70(10): 812-813.
66. Zivadinov R, Bastianello S, Dake MD, et al. Recommendations for multimodal noninvasive and invasive screening for detection of extracranial venous abnormalities indicative of chronic cerebrospinal venous insufficiency: a position statement of the International Society for Neurovascular Disease. J Vasc Interv Radiol, 2014, 25(11): 1785-1794.e17.
67. Caprio MG, Marr K, Gandhi S, et al. Centralized and local color doppler ultrasound reading agreement for diagnosis of the chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. Curr Neurovasc Res, 2017, 14(3): 266-273.
68. Scalise F, Novelli E, Farina M, et al. Venous hemodynamic insufficiency severity score variation after endovascular treatment of chronic cerebrospinal venous insufficiency. Phlebology, 2015, 30(4): 250-256.
69. Zamboni P, Menegatti E, Cittanti C, et al. Fixing the jugular flow reduces ventricle volume and improves brain perfusion. J Vasc Surg Venous Lymphat Disord, 2016, 4(4): 434-445.
70. Sadovnick AD, Yee IM, Attwell-Pope K, et al. Patient-Reported benefits of extracranial venous therapy: British Columbia CCSVI registry. Can J Neurol Sci, 2017, 44(3): 246-254.

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