Indicators of cerebral venous drainage with non-thrombotic disorders in extracranial veins
https://doi.org/10.18699/SSMJ20240108
Abstract
The growing number of studies on cerebral venous circulation disorders associated with extrinsic stenosis of the internal jugular veins, as well as attempts to surgically influence the restoration of blood flow, are an indicator of the importance of this problem. Studies show that extracranial outflow disorders are associated with a wide range of neurological clinical manifestations and may contribute to the development of congestive intracranial hypertension. Anatomical variants of the development of the extracranial venous system, constitutional insufficiency and stenosis often play similar roles in the development of disorders of the cerebral venous outflow, but differ parametrically. There are no standard diagnostic criteria for differential diagnosis, normal and pathological parameters are contradictory, and the diagnosis largely depends on the combined use of imaging techniques. The history of attempts to study disorders of the cerebral venous circulation is quite long, associated with the technical innovations in every period of time. The most non-invasive, accessible and safe tools for diagnosing non-thrombotic lesions and anomalies of the internal jugular veins are currently recognized as ultrasound scanning and MR venography in tandem. Researchers note both local hemodynamic disturbances at the level of stenosis and changes in the overall picture of the venous vascular network of the neck with certain patterns of its remodeling. The pathological significance of the compensatory expansion of nonjugular outflow tracts (vertebral, paraspinal collateral, spinal epidural veins, etc.) is still a controversial issue. MRI and ultrasound combined show a high degree of agreement between the results, which should stimulate further research into the pathophysiology and differentiation of various causes and severity of non-thrombotic lesions of the jugular veins.
Keywords
About the Authors
S. E. SemenovRussian Federation
Stanislav E. Semenov, doctor of medical sciences
650002, Kemerovo, Sosnoviy вlvd., 6
D. V. Bondarchuk
Russian Federation
Dmitriy V. Bondarchuk
127051, Moscow, Petrovka st., 24/1
A. N. Kokov
Russian Federation
Alexandr N. Kokov, candidate of medical sciences
650002, Kemerovo, Sosnoviy вlvd., 6
M. G. Shatokhina
Russian Federation
Maria G. Shatokhina, candidate of medical sciences
197341, Saint Petersburg, Akkuratova st., 2
References
1. Zhou D., Meng R., Zhang X., Guo L., Li S., Wu W., Duan J., Song H., Ding Y., Ji X. Intracranial hypertension induced by internal jugular vein stenosis can be resolved by stenting. Eur. J. Neurol. 2018;25(2):365-e13. doi: 10.1111/ene.13512
2. Semenov S.E., Shatokhina M.G., Bondarchuk D.V., Moldavskaya I.V. On the problem of diagnosing the initial manifestations of insufficiency of cerebral venous circulation. Klinicheskaya fiziologiya krovoobrashcheniya = Clinical Physiology of Circulation. 2022;19(3):266–279. [In Russian]. doi: 10.24022/1814-6910-2022-1
3. Bateman A.R., Bateman G.A., Barber T. The relationship between cerebral blood flow and venous sinus pressure: can hyperemia induce idiopathic intracranial hypertension? Fluids Barriers CNS. 2021;18(1):5. doi: 10.1186/s12987-021-00239-2
4. Moldavskaya I.V. Radiological criteria for brachiocephalic vein stenosis and clinical severity of cerebral venous stasis: abstract of thesis….cand. med. sci. Tomsk, 2013. [In Russian].
5. Dollinger P., Böhm J., Arányi Z. Combined nerve and vascular ultrasound in thoracic outlet syndrome: A sensitive method in identifying the site of neurovascular compression. PLoS One. 2022;17(5):e0268842. doi: 10.1371/journal.pone.0268842
6. Shumilina M.V. Ultrasound examinations for headaches in patients with cardiovascular pathology. Moscow: NMITSSSKH im. A.N. Bakuleva, 2022. 78 p. [In Russian].
7. Alekseev V.V., Shekhter A.I., Skorobogatykh K.V., Shashkova E.V. Headaches due to intracranial venous dysfunction. Bol’ = The pain. 2008;(3):15–21. [In Russian].
8. Semenov S.E., Kovalenko A.V., Moldavskaya I.V., Khromov A.A., Zhuchkova E.A., Khromova A.N., Semenov A.S. Diagnosis and role of cerebral venous congestion in the course and outcome of non-hemorrhagic stroke. Kompleksnyye problemy serdechno-sosudistykh zabolevaniy = Complex Issues of Cardiovascular Diseases. 2014;(3):108–117. [In Russian]. doi: 10.17802/2306-1278-2014-3-108-117
9. Berdichevskiy M.Ya. Venous discirculatory pathology of the brain. Moscow: Meditsina, 1989. 224 p. [In Russian].
10. Vascular diseases of the nervous system. Ed. E.V. Shmidt. Moscow: Meditsina, 1975. 664 p. [In Russian].
11. Verulashvili I., Beraya M., Kortushvili M. Features of cerebral venous hemodynamics in chronic cerebrovascular accidents. Effektivnaya farmakoterapiya = Effective pharmacotherapy. 2018;24:88–92. [In Russian].
12. Semenov S.E., Moldavskaya I.V., Kovalenko A.V., Khromov A.A., Khromova A.N., Zhuchkova E.A., Portnov Yu.M., Kokov A.N. Radiological criteria for stenosis of the brachiocephalic veins and the clinical severity of cerebral venous stasis. Klinicheskaya fiziologiya krovoobrashcheniya = Clinical Physiology of Circulation. 2013;(2):35–44. [In Russian].
13. Nazarova Zh.A., Bahadirkhanov M.M. Features of venous cerebral hemodynamics in acute cerebrovascular accidents. Vestnik ekstrennoy meditsiny = The Bulletin of Emergency Medicine. 2019;12(6):35–41. [In Russian].
14. Ahn S.S., Miller T.J., Chen S.W., Chen J.F. Internal jugular vein stenosis is common in patients presenting with neurogenic thoracic outlet syndrome. Ann. Vasc. Surg. 2014;28(4):946–50. doi: 10.1016/j.avsg.2013.12.009
15. Ding J.Y., Zhou D., Pan L.Q., Ya J.Y., Liu C., Yan F., Fan C.Q., Ding Y.C., Ji X.M., Meng R. Cervical spondylotic internal jugular venous compression syndrome. CNS Neurosci. Ther. 2020;26(1):47–54. doi: 10.1111/cns.13148
16. Li M., Sun Y., Chan C.C., Fan C., Ji X., Meng R. Internal jugular vein stenosis associated with elongated styloid process: five case reports and literature review. BMC Neurol. 2019;19(1):112. doi: 10.1186/s12883-019-1344-0
17. Rashid A., Iqrar S.A., Rashid A., Simka M. Results of numerical modeling of blood flow in the internal jugular vein exhibiting different types of strictures. Diagnostics (Basel). 2022;12(11):2862. doi: 10.3390/diagnostics12112862
18. Dashti S.R., Nakaji P., Hu Y.C., Frei D.F., Abla A.A., Yao T., Fiorella D. Styloidogenic jugular venous compression syndrome: diagnosis and treatment: case report. Neurosurgery. 2012;70(3):E795–799. doi: 10.1227/NEU.0b013e3182333859
19. Higgins J.N., Garnett M.R., Pickard J.D., Axon P.R. An evaluation of styloidectomy as an adjunct or alternative to jugular stenting in idiopathic intracranial hypertension and disturbances of cranial venous outflow. J. Neurol. Surg. B. Skull. Base. 2017;78(2):158–163. doi: 10.1055/s-0036-1594238
20. Oushy S., Wald J.T., Janus J., Fulgham J.R., Lanzino G. Dynamic internal jugular vein compression by hypertrophic hyoid bone: management and outcomes. Cureus. 2020;12(3):e7445. doi: 10.7759/cureus.7445
21. Semenov S.E. Noninvasive radiodiagnosis of obstructive disorders of cerebral venous circulation: abstract of thesis… doct. med. sci. Tomsk, 2003. [In Russian].
22. Serousova O.V., Karpova M.I., Nadtochiy N.B., Korotkova D.G., Vasilenko A.F. Neuroimaging for headache: possible findings and their interpretation. Rossiyskiy zhurnal boli = Russian Journal of Pain. 2022;20(3):52–61 [In Russian] doi: 10.17116/pain20222003152
23. Nicholson P., Kedra A., Shotar E., Bonnin S., Boch A.L., Shor N., Clarençon F., Touitou V., Lenck S. Idiopathic intracranial hypertension: glymphedema of the brain. J. Neuroophthalmol. 2021;41(1):93–97. doi: 10.1097/WNO.0000000000001000
24. Semenov S.E., Bondarchuk D.V., Malkov I.N., Shatokhina M.G. Ultrasound and magnetic resonance of extrinsic stenosis and hypoplasia of internal jugular veins. Kompleksnyye problemy serdechno-sosudistykh zabolevaniy = Complex Issues of Cardiovascular Diseases. 2023;12(1):72–83. [In Russian]. doi: 10.17802/2306-1278-2023-12-1-72-83
25. Friedman D.I., Liu G.T., Digre K.B. Revised diagnostic criteria for the pseudotumor cerebri syndrome in adults and children. Neurology. 2013;81(13):1159–1165. doi: 10.1212/WNL.0b013e3182a55f17
26. Ferro J.M., Canhao P., Stam J., Bousser M.G., Barinagarrementeria F.; ISCVT Investigators. Prognosis of cerebral vein and dural sinus thrombosis: results of the International Study on Cerebral Vein and Dural Sinus Thrombosis (ISCVT). Stroke. 2004;35(3):664–670. doi: 10.1161/01.STR.0000117571.76197.26
27. Dolic K., Siddiqui A.H., Karmon Y., Marr K., Zivadinov R. The role of noninvasive and invasive diagnostic imaging techniques for detection of extracranial venous system anomalies and developmental variants. BMC Med. 2013;11:155. doi: 10.1186/1741-7015-11-155
28. Shumilina M.V., Arakelyan V.S., Darvish N.A., Ozolinsh A.A. On the problem of studying arterial and venous circulation in patients. Klinicheskaya fiziologiya krovoobrashcheniya = Clinical Physiology of Circulation. 2018;15(1):50–53. [In Russian].
29. Myerson A., Loman J. Internal jugular venous pressure in men, its relationship to cerebrospinal fluid and carotid arterial pressures. Arch. Neurol. Psychiatry. 1932;27(4):836–846. doi: 10.1001/archneurpsyc.1932.02230160077008
30. Shumilina M.V., Makhmudov Kh.Kh., Mukaseyeva A.V., Strelkova T.V. Method for measuring venous pressure. Patent 2480149 RF; published 27.04.2013. [In Russian].
31. Semenov S., Yurkevich E., Semenov A. Determination of indicator model of cerebral venous thrombosis by using brachiocephalic vessels ultrasound index of arteriovenous ratio and headache visual analogue scale. Recent Developments in Medicine and Medical Research. 2021;15:18–28. doi: 10.9734/bpi/rdmmr/v15/15014D
32. Shumilina M.V. Disturbances of cerebral venous circulation in patients with cardiovascular pathology: аbstract of thesis … doct. med. sci. Moscow, 2002. [In Russian].
33. Mohammadyari P., Gadda G., Taibi A. Modelling physiology of haemodynamic adaptation in shortterm microgravity exposure and orthostatic stress on Earth. Sci. Rep. 2021;11(1):4672. doi: 10.1038/s41598-021-84197-7
34. Semenov S.E., Burdin S.N., Bukhtoyarova V.I., Moldavskaya I.V., Sizova I.N., Ten S.B. Ultrasound criteria for the hemodynamic significance of obstruction of the brachiocephalic veins. Klinicheskaya fiziologiya krovoobrashcheniya = Clinical Physiology of Circulation. 2009;(3):42–50. [In Russian].
35. Han K., Chao A.C., Chang F.C., Chung C.P., Hsu H.Y., Sheng W.Y., Wu J., Hu H.H. Obstruction of venous drainage linked to transient global amnesia. PLoS One. 2015;10(7):e0132893. doi: 10.1371/journal.pone.0132893
36. Smolock E., Berk B.C. Chapter 98 – Vascular smooth muscle cell remodeling in atherosclerosis and restenosis. Muscle. 2012;2:1301–1309. doi: 10.1016/B978-0-12-381510-1.00098-3
37. Magnano C., Belov P., Krawiecki J., Hagemeier J., Beggs C., Zivadinov R. Internal jugular vein cross–sectional area enlargement is associated with aging in healthy individuals. PLoS ONE. 2016;11(2):e0149532. doi: 10.1371/journal.pone.0149532
38. Doepp F., Schreiber S.J., von Münster T., Rademacher J., Klingebiel R., Valdueza J.M. How does the blood leave the brain? A systematic ultrasound analysis of cerebral venous drainage patterns. Neuroradiology. 2004;46(7):565–570. doi: 10.1007/s00234-004-1213-3
39. Tanoue S., Kiyosue H., Sagara Y., Hori Y., Okahara M., Kashiwagi J., Mori H. Venous structures at the craniocervical junction: anatomical variations evaluated by multidetector row CT. Br. J. Radiol. 2010;83(994):831–840. doi: 10.1259/bjr/85248833
40. 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. doi: 10.1016/j.brainresrev.2004.04.005
41. Zamboni P., Consorti G., Galeotti R., Gianesini S., Menegatti E., Tacconi G., Carinci F. Venous collateral circulation of the extracranial cerebrospinal outflow routes. Curr. Neurovasc. Res. 2009;6(3):204–212. doi: 10.2174/156720209788970054
42. Thibault P., Lewis W., Niblett S. Objective duplex ultrasound evaluation of the extracranial circulation in multiple sclerosis patients undergoing venoplasty of internal jugular vein stenoses: a pilot study. Phlebology. 2015;30(2):98–104. doi: 10.1177/0268355513515473
43. Gadda G., Taibi A., Sisini F., Gambaccini M., Sethi S.K., Utriainen D.T., Haacke E.M., Zamboni P., Ursino M. Validation of a hemodynamic model for the study of the cerebral venous outflow system using MR imaging and echo-color Doppler data. AJNR Am. J. Neuroradiol. 2016;37(11):2100–2109. doi: 10.3174/ajnr.A4860
44. Traboulsee A.L., Knox K.B., Machan L., Zhao Y., Yee I., Rauscher A., Klass D., Szkup P., Otani R., Kopriva D., Lala S., Li D.K., Sadovnick D. 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. doi: 10.1016/S0140-6736(13)61747-X
45. Ding J.Y., Zhou D., Pan L.Q., Ya J.Y., Liu C., Yan F., Fan C.Q., Ding Y.C., Ji X.M., Meng R. Cervical spondylotic internal jugular venous compression syndrome. CNS Neurosci. Ther. 2020;26(1):47–54. doi: 10.1111/cns.13148
46. Wang Z., Ding J., Bai C., Ding Y., Ji X., Meng R. Clinical classification and collateral circulation in chronic cerebrospinal venous insufficiency. Front. Neurol. 2020;11:913. doi: 10.3389/fneur.2020.00913
47. Marr K., Jakimovski D., Mancini M., Carl E., Zivadinov R. Jugular venous flow quantification using Doppler sonography. Ultrasound. Med. Biol. 2018;44(8):1762–1769. doi: 10.1016/j.ultrasmedbio.2018.04.010
48. Karmon Y., Zivadinov R., Weinstock-Guttman B., Marr K., Valnarov V., Dolic K., Kennedy C.L., Hojnacki D., Carl E.M., Hagemeier J., Hopkins L.N., Levy E.I., Siddiqui A.H. Comparison of intravascular ultrasound with conventional venography for detection of extracranial venous abnormalities indicative of chronic cerebrospinal venous insufficiency. J. Vasc. Interv. Radiol. 2013;24(10):1487–1498.e1. doi: 10.1016/j.jvir.2013.06.012
49. Scalise F., Farina M., Manfredi M., Auguadro C., Novelli E. Assessment of jugular endovascular malformations in chronic cerebrospinal venous insufficiency: colour-Doppler scanning and catheter venography compared with intravascular ultrasound. Phlebology. 2013;28(8):409–417. doi: 10.1258/phleb.2012.012079
50. Roberts G.S., Peret A., Jonaitis E.M., Koscik R.L., Hoffman C.A., Rivera-Rivera L.A., Cody K.A., Rowley H.A., Johnson S.C., Wieben O., Johnson K.M., Eisenmenger L.B. Normative cerebral hemodynamics in middle-aged and older adults using 4D flow MRI: initial analysis of vascular aging. Radiology. 2023;307(3):e222685. doi: 10.1148/radiol.222685
51. Sethi S.K., Daugherty A.M., Gadda G., Utriainen D.T., Jiang J., Raz N., Haacke E.M. Jugular anomalies in multiple sclerosis are associated with increased collateral venous flow. AJNR Am. J. Neuroradiol. 2017;38(8):1617–1622. doi: 10.3174/ajnr.A5219
52. Savelyeva L.A., Tulupov A.A. Features of venous outflow from the brain, according to magnetic resonance angiography. Vestnik Novosibirskogo gosudarstvennogo universiteta. Seriya: biologiya, clinicheskaya meditsina = Vestnik NSU. Series: Biology, clinical medicine. 2009;7(1):36–40. [In Russian]
53. İlhan Z., Açıkgözoğlu S., Demir O. Associations between Doppler internal jugular vein blood flow and transverse sinus stasis detected by magnetic resonance imaging. J. Ultrasound. Med. 2021;40(8):1591–1601. doi: 10.1002/jum.15541
54. Zamboni P., Menegatti E., Cittanti C., Sisini F., Gianesini S., Salvi F., Mascoli F. Fixing the jugular flow reduces ventricle volume and improves brain perfusion. J. Vasc. Surg. Venous Lymphat. Disord. 2016;4(4):434–445. doi: 10.1016/j.jvsv.2016.06.006
55. Torres C., Hogan M., Patro S., Chakraborty S., Nguyen T., Thornhill R., Freedman M., Bussiere M., Dabirzadeh H., Schwarz B.A., Belanger S., Legault-Kingstone L., Schweitzer M., Lum C. Extracranial venous abnormalities: a true pathological finding in patients with multiple sclerosis or an anatomical variant? Eur. Radiol. 2017;27(1):239–246. doi: 10.1007/s00330-016-4314-6
56. El Sankari S., Gondry-Jouet C., Fichten A., Godefroy O., Serot J.M., Deramond H., Meyer M.E., Balédent O. Cerebrospinal fluid and blood flow in mild cognitive impairment and Alzheimer’s disease: a differential diagnosis from idiopathic normal pressure hydrocephalus. Fluids Barriers CNS. 2011;8(1):12. doi: 10.1186/2045-8118-8-12
57. Zivadinov R., Poloni G.U., Marr K., Schirda C.V., Magnano C.R., Carl E., Bergsland N., Hojnacki D., Kennedy C., Beggs C.B., Dwyer M.G., Weinstock-Guttman B. Decreased brain venous vasculature visibility on susceptibility-weighted imaging venography in patients with multiple sclerosis is related to chronic cerebrospinal venous insufficiency. BMC Neurol. 2011;11:128. doi: 10.1186/1471-2377-11-128
58. Semenov S.E. Radiologic diagnosis of venous ischemic stroke. Saint-Petersburg: Foliant, 2018. 216 p. [In Russian].
59. Zamboni P., Menegatti E., Weinstock-Guttman B., Dwyer M.G., Schirda C.V., Malagoni A.M., Hojnacki D., Kennedy C., Carl E., Bergsland N., Magnano C., Bartolomei I., Salvi F., Zivadinov R. 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. 2011;9:22. doi: 10.1186/1741-7015-9-22
60. Garaci F.G., Marziali S., Meschini A., Fornari M., Rossi S., Melis M., Fabiano S., Stefanini M., Simonetti G., Centonze D., Floris R. Brain hemodynamic changes associated with chronic cerebrospinal venous insufficiency are not specific to multiple sclerosis and do not increase its severity. Radiology. 2012;265(1):233–239. doi: 10.1148/radiol.12112245
61. Semenov S.E., Yurkevich E.A., Moldavskaia I.V., Shatokhina M.G., Semenov A.S. Diagnosis of venous ischemic stroke. Part II (algorithms and semiology of diagnostic radiology. Limitations in clinical practice). A review. Kompleksnyye problemy serdechno-sosudistykh zabolevaniy = Complex Issues of Cardiovascular Diseases. 2019;8(3):104–115. [In Russian]. doi: 10.17802/2306-1278-2019-8-3-104-115
62. Kefayati S., Amans M., Faraji F., Ballweber M., Kao E., Ahn S., Meisel K., Halbach V., Saloner D. The manifestation of vortical and secondary flow in the cerebral venous outflow tract: An in vivo MR velocimetry study. J. Biomech. 2017;50:180–187. doi: 10.1016/j.jbiomech.2016.11.041
63. Jayaraman M.V., Boxerman J.L., Davis L.M., Haas R.A., Rogg J.M. Incidence of extrinsic compression of the internal jugular vein in unselected patients undergoing CT angiography. AJNR Am. J. Neuroradiol. 2012;33(7):1247–1250. doi: 10.3174/ajnr.A2953
Review
For citations:
Semenov S.E., Bondarchuk D.V., Kokov A.N., Shatokhina M.G. Indicators of cerebral venous drainage with non-thrombotic disorders in extracranial veins. Сибирский научный медицинский журнал. 2024;44(1):76-87. (In Russ.) https://doi.org/10.18699/SSMJ20240108