Enlarged Perivascular Space in the Basal Ganglia is Associated with Cerebral Venous Reflux in Patients with Recent Small Subcortical Infarction


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Abstract

Background:Research has linked enlarged perivascular spaces (EPVS) to cerebral venous reflux (CVR) in patients with hypertensive intracerebral hemorrhage, but it is unclear whether this association exists in recent small subcortical infarct (RSSI) patients.

Objective:This study aimed to investigate the correlation between EPVS and CVR in patients with RSSI.

Method:This study included 297 patients, selected from patients with RSSI in the lenticulostriate artery admitted to the Department of Neurology of the First Affiliated Hospital of Zhengzhou University. CVR was assessed by time-of-flight magnetic resonance angiography (TOF-MRA). The relationship between EPVS and CVR was studied using multiple logistic regression analysis.

Results:This study included patients with an average age of 59.84±12.27 years, including 201 males (67.7%). CVR was observed in 40 (13.5%) patients. Compared to the group without CVR, the proportions of male patients and patients with a history of smoking and drinking were higher in the CVR group. The proportions of high-grade EPVS in the centrum semiovale region [23 cases (57.5%) vs. 108 cases (42.0%), p =0.067] and the basal ganglia region [30 cases (75.0%) vs. 133 cases (51.8%), p =0.006] were higher in the CVR group. After multiple logistic regression analysis, high-grade EPVS in the basal ganglia region was still associated with CVR (OR, 2.68; 95% CI, 1.22-5.87; p =0.014).

Conclusion:In the population with RSSI, EPVS in basal ganglia is significantly associated with CVR, suggesting a close relationship between venous dysfunction and the formation of EPVS.

About the authors

Zhengrong Wu

Department of Neurology, The First Affiliated Hospital of Zhengzhou University

Email: info@benthamscience.net

Ke Zhang

Department of Neurology, The First Affiliated Hospital of Zhengzhou University

Email: info@benthamscience.net

Ce Zong

Department of Neurology, The First Affiliated Hospital of Zhengzhou University

Email: info@benthamscience.net

Hongbing Liu

Department of Neurology, The First Affiliated Hospital of Zhengzhou University

Email: info@benthamscience.net

Yanhong Wang

Department of Neurology, The First Affiliated Hospital of Zhengzhou University

Email: info@benthamscience.net

Yuming Xu

Department of Neurology, The First Affiliated Hospital of Zhengzhou University

Email: info@benthamscience.net

Yuan Gao

Department of Neurology, The First Affiliated Hospital of Zhengzhou University

Author for correspondence.
Email: info@benthamscience.net

References

  1. 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): 243-60. doi: 10.1016/j.brainresrev.2004.04.005 PMID: 15571768
  2. Fulop GA, Tarantini S, Yabluchanskiy AJAJOP. Role of age-related alterations of the cerebral venous circulation in the pathogenesis of vascular cognitive impairment. Am J Physiol Heart Circ Physiol 2019; (5 Pt.2): 316.
  3. 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): 601-9. doi: 10.3233/JAD-131112 PMID: 24217278
  4. Chung CP, Hu HH. Pathogenesis of leukoaraiosis: Role of jugular venous reflux. Med Hypotheses 2010; 75(1): 85-90. doi: 10.1016/j.mehy.2010.01.042 PMID: 20172657
  5. Tsai HH, Lee BC, Chen YF, Jeng JS, Tsai LK. Cerebral venous reflux and dilated basal ganglia perivascular space in hypertensive intracerebral hemorrhage. J Stroke 2022; 24(3): 363-71. doi: 10.5853/jos.2022.01004 PMID: 36221939
  6. Mestre H, Kostrikov S, Mehta RI, Nedergaard M. Perivascular spaces, glymphatic dysfunction, and small vessel disease. Clin Sci 2017; 131(17): 2257-74. doi: 10.1042/CS20160381 PMID: 28798076
  7. Yu L, Hu X, Li H, Zhao Y. Perivascular spaces, glymphatic system and MR. Front Neurol 2022; 13: 844938. doi: 10.3389/fneur.2022.844938 PMID: 35592469
  8. Ramaswamy S, Khasiyev F, Gutierrez J. Brain enlarged perivascular spaces as imaging biomarkers of cerebrovascular disease: A clinical narrative review. J Am Heart Assoc 2022; 11(24): e026601. doi: 10.1161/JAHA.122.026601 PMID: 36533613
  9. Lee BC, Tsai HH, Liu CJ, et al. Cerebral venous reflux and cerebral amyloid angiopathy: An magnetic resonance imaging/positron emission tomography study. Stroke 2023; 54(4): 1046-55. doi: 10.1161/STROKEAHA.122.040503 PMID: 36866674
  10. Kim JS, Yoon Y. Single subcortical infarction associated with parental arterial disease: Important yet neglected sub-type of atherothrombotic stroke. Int J Stroke 2013; 8(3): 197-203. doi: 10.1111/j.1747-4949.2012.00816.x PMID: 22568537
  11. Caton MT, Callen AL, Copelan AZ, Narsinh KH, Smith ER, Amans MR. Jugular venous reflux can mimic posterior fossa dural arteriovenous fistulas on MRI-MRA. AJR Am J Roentgenol 2021; 216(6): 1626-33. doi: 10.2214/AJR.20.24012 PMID: 32876481
  12. Uchino A, Nomiyama K, Takase Y, et al. Retrograde flow in the dural sinuses detected by three-dimensional time-of-flight MR angiography. Neuroradiology 2007; 49(3): 211-5. doi: 10.1007/s00234-006-0186-9 PMID: 17180368
  13. Jang J, Kim B, Kim B, et al. Reflux venous flow in dural sinus and internal jugular vein on 3D time-of-flight MR angiography. Neuroradiology 2013; 55(10): 1205-11. doi: 10.1007/s00234-013-1239-5 PMID: 23868180
  14. Lee J, Lee JY, Lee YJ, et al. Differentiation of dural arteriovenous fistula from reflux venous flow on 3D TOF-MR angiography: Identifying asymmetric enlargement of external carotid artery branches. Clin Radiol 2020; 75(9): 714.e15-20.
  15. Kim E, Kim JH, Choi BS, Jung C, Lee DH. MRI and MR angiography findings to differentiate jugular venous reflux from cavernous dural arteriovenous fistula. AJR Am J Roentgenol 2014; 202(4): 839-46. doi: 10.2214/AJR.13.11048 PMID: 24660714
  16. Wardlaw JM, Smith EE, Biessels GJ, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 2013; 12(8): 822-38. doi: 10.1016/S1474-4422(13)70124-8 PMID: 23867200
  17. Xu Z, Li F, Wang B, et al. New insights in addressing cerebral small vessel disease: Association with the deep medullary veins. Front Aging Neurosci 2020; 12: 597799. doi: 10.3389/fnagi.2020.597799 PMID: 33335483
  18. Gregoire SM, Chaudhary UJ, Brown MM, et al. The microbleed anatomical rating scale (MARS): Reliability of a tool to map brain microbleeds. Neurology 2009; 73(21): 1759-66. doi: 10.1212/WNL.0b013e3181c34a7d PMID: 19933977
  19. Cordonnier C, Potter GM, Jackson CA, et al. improving interrater agreement about brain microbleeds: Development of the Brain Observer MicroBleed Scale (BOMBS). Stroke 2009; 40(1): 94-9. doi: 10.1161/STROKEAHA.108.526996 PMID: 19008468
  20. Kapeller P, Barber R, Vermeulen RJ, et al. Visual rating of age-related white matter changes on magnetic resonance imaging: scale comparison, interrater agreement, and correlations with quantitative measurements. Stroke 2003; 34(2): 441-5. doi: 10.1161/01.STR.0000049766.26453.E9 PMID: 12574557
  21. Jessen NA, Munk ASF, Lundgaard I, Nedergaard M. The glymphatic system: A beginner’s guide. Neurochem Res 2015; 40(12): 2583-99. doi: 10.1007/s11064-015-1581-6 PMID: 25947369
  22. Gouveia-Freitas K, Bastos-Leite AJ. Perivascular spaces and brain waste clearance systems: Relevance for neurodegenerative and cerebrovascular pathology. Neuroradiology 2021; 63(10): 1581-97. doi: 10.1007/s00234-021-02718-7 PMID: 34019111
  23. Brown R, Benveniste H, Black SE, et al. Understanding the role of the perivascular space in cerebral small vessel disease. Cardiovasc Res 2018; 114(11): 1462-73. doi: 10.1093/cvr/cvy113 PMID: 29726891
  24. Waragai M, Takeuchi H, Fukushima T, Haisa T, Yonemitsu T. MRI and SPECT studies of dural arteriovenous fistulas presenting as pure progressive dementia with leukoencephalopathy: A cause of treatable dementia. Eur J Neurol 2006; 13(7): 754-9. doi: 10.1111/j.1468-1331.2006.01318.x PMID: 16834706
  25. 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): 553-9. doi: 10.1002/ana.22276 PMID: 21391231
  26. Tanaka T, Uemura K, Takahashi M, et al. Compression of the left brachiocephalic vein: Cause of high signal intensity of the left sigmoid sinus and internal jugular vein on MR images. Radiology 1993; 188(2): 355-61. doi: 10.1148/radiology.188.2.8327678 PMID: 8327678
  27. Saiki K, Tsurumoto T, Okamoto K, Wakebe T. Relation between bilateral differences in internal jugular vein caliber and flow patterns of dural venous sinuses. Anat Sci Int 2013; 88(3): 141-50. doi: 10.1007/s12565-013-0176-z PMID: 23572397

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