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    An overview of cerebral venules: From structure, pathology, and imaging to related diseases

    • Pei Wang
    • Yuan Cao
    • Yi-Cheng Zhu


    Abstract

    The cerebral microvascular system, which includes arterioles, capillaries, and venules, has often been studied as a whole in the past. Compared to the small arteries, we know very little about cerebral venules. Venous collagenosis was first proposed by Moody in 1995. With the development of imaging techniques, we can visualize cerebral venules in vivo by susceptibility-weighted imaging. There is a growing evidence that cerebral venules are associated with related neurological disorders such as cerebral small vessel disease, Alzheimer's disease, and multiple sclerosis. However, the risk factors leading to functional and structural alterations in the cerebral venules and the associated pathogenic mechanisms are not yet known. In this article, we review and summarize the studies related to cerebral venules.

    Keywords: cerebral venules anatomy pathology imaging neurological disorders
    Section

    References

    1. Adams, C. W. (1988). Perivascular iron deposition and other vascular damage in multiple sclerosis. J Neurol Neurosurg Psychiatry, 51(2), 260-265. doi:10.1136/jnnp.51.2.260
    2. Adams, C. W., Poston, R. N., Buk, S. J., Sidhu, Y. S., & Vipond, H. (1985). Inflammatory vasculitis in multiple sclerosis. J Neurol Sci, 69(3), 269-283. doi:10.1016/0022-510x(85)90139-x
    3. Amin Al Olama, A., Wason, J. M. S., Tuladhar, A. M., van Leijsen, E. M. C., Koini, M., Hofer, E., . . . Markus, H. S. (2020). Simple MRI score aids prediction of dementia in cerebral small vessel disease. Neurology, 94(12), e1294-e1302. doi:10.1212/WNL.0000000000009141
    4. Ao, D. H., Zhang, D. D., Zhai, F. F., Zhang, J. T., Han, F., Li, M. L., . . . Zhu, Y. C. (2021). Brain deep medullary veins on 3-T MRI in a population-based cohort. J Cereb Blood Flow Metab, 41(3), 561-568. doi:10.1177/0271678X20918467
    5. Bakkour, A., Morris, J. C., Wolk, D. A., & Dickerson, B. C. (2013). The effects of aging and Alzheimer's disease on cerebral cortical anatomy: specificity and differential relationships with cognition. Neuroimage, 76, 332-344. doi:10.1016/j.neuroimage.2013.02.059
    6. Bernier, M., Cunnane, S. C., & Whittingstall, K. (2018). The morphology of the human cerebrovascular system. Hum Brain Mapp, 39(12), 4962-4975. doi:10.1002/hbm.24337
    7. Black, S., Gao, F., & Bilbao, J. (2009). Understanding white matter disease: imaging-pathological correlations in vascular cognitive impairment. Stroke, 40(3 Suppl), S48-52. doi:10.1161/STROKEAHA.108.537704
    8. Blair, G. W., Thrippleton, M. J., Shi, Y., Hamilton, I., Stringer, M., Chappell, F., . . . Wardlaw, J. M. (2020). Intracranial hemodynamic relationships in patients with cerebral small vessel disease. Neurology, 94(21), e2258-e2269. doi:10.1212/WNL.0000000000009483
    9. Bouvy, W. H., Kuijf, H. J., Zwanenburg, J. J., Koek, H. L., Kappelle, L. J., Luijten, P. R., . . . Utrecht Vascular Cognitive Impairment Study, g. (2017). Abnormalities of Cerebral Deep Medullary Veins on 7 Tesla MRI in Amnestic Mild Cognitive Impairment and Early Alzheimer's Disease: A Pilot Study. J Alzheimers Dis, 57(3), 705-710. doi:10.3233/JAD-160952
    10. Brown, S. R., Cleveland, E. M., Deeken, C. R., Huitron, S. S., Aluka, K. J., & Davis, K. G. (2017). Type I/type III collagen ratio associated with diverticulitis of the colon in young patients. J Surg Res, 207, 229-234. doi:10.1016/j.jss.2016.08.044
    11. Brown, W. R., Moody, D. M., Challa, V. R., Thore, C. R., & Anstrom, J. A. (2002). Venous collagenosis and arteriolar tortuosity in leukoaraiosis. J Neurol Sci, 203-204, 159-163. doi:10.1016/s0022-510x(02)00283-6
    12. Brown, W. R., Moody, D. M., Thore, C. R., Anstrom, J. A., & Challa, V. R. (2009). Microvascular changes in the white mater in dementia. J Neurol Sci, 283(1-2), 28-31. doi:10.1016/j.jns.2009.02.328
    13. Brown, W. R., & Thore, C. R. (2011). Review: cerebral microvascular pathology in ageing and neurodegeneration. Neuropathol Appl Neurobiol, 37(1), 56-74. doi:10.1111/j.1365-2990.2010.01139.x
    14. Cao, Y., Ao, D. H., Ma, C., Qiu, W. Y., & Zhu, Y. C. (2021). Immunoreactivity and a new staining method of monocarboxylate transporter 1 located in endothelial cells of cerebral vessels of human brain in distinguishing cerebral venules from arterioles. Eur J Histochem, 65(s1). doi:10.4081/ejh.2021.3306
    15. Cao, Y., Huang, M. Y., Mao, C. H., Wang, X., Xu, Y. Y., Qian, X. J., . . . Zhu, Y. C. (2022). Arteriolosclerosis differs from venular collagenosis in relation to cerebrovascular parenchymal damages: an autopsy-based study. Stroke Vasc Neurol. doi:10.1136/svn-2022-001924
    16. Chen, X., Wei, L., Wang, J., Shan, Y., Cai, W., Men, X., . . . Wu, A. (2020). Decreased visible deep medullary veins is a novel imaging marker for cerebral small vessel disease. Neurol Sci, 41(6), 1497-1506. doi:10.1007/s10072-019-04203-9
    17. Cheung, C. Y., Ong, Y. T., Ikram, M. K., Ong, S. Y., Li, X., Hilal, S., . . . Wong, T. Y. (2014). Microvascular network alterations in the retina of patients with Alzheimer's disease. Alzheimers Dement, 10(2), 135-142. doi:10.1016/j.jalz.2013.06.009
    18. Cohen, R. M., Rezai-Zadeh, K., Weitz, T. M., Rentsendorj, A., Gate, D., Spivak, I., . . . Town, T. (2013). A transgenic Alzheimer rat with plaques, tau pathology, behavioral impairment, oligomeric abeta, and frank neuronal loss. J Neurosci, 33(15), 6245-6256. doi:10.1523/JNEUROSCI.3672-12.2013
    19. Compston, A., & Coles, A. (2008). Multiple sclerosis. Lancet, 372(9648), 1502-1517. doi:10.1016/S0140-6736(08)61620-7
    20. Dahl, E. (1973). The fine structure of intracerebral vessels. Z Zellforsch Mikrosk Anat, 145(4), 577-586. doi:10.1007/BF00306725
    21. De Guio, F., Vignaud, A., Ropele, S., Duering, M., Duchesnay, E., Chabriat, H., & Jouvent, E. (2014). Loss of venous integrity in cerebral small vessel disease: a 7-T MRI study in cerebral autosomal-dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL). Stroke, 45(7), 2124-2126. doi:10.1161/STROKEAHA.114.005726
    22. Friedman, D. P. (1997). Abnormalities of the deep medullary white matter veins: MR imaging findings. AJR Am J Roentgenol, 168(4), 1103-1108. doi:10.2214/ajr.168.4.9124123
    23. Gatseva, A., Sin, Y. Y., Brezzo, G., & Van Agtmael, T. (2019). Basement membrane collagens and disease mechanisms. Essays Biochem, 63(3), 297-312. doi:10.1042/EBC20180071
    24. Ge, Y., Zohrabian, V. M., Osa, E. O., Xu, J., Jaggi, H., Herbert, J., . . . Grossman, R. I. (2009). Diminished visibility of cerebral venous vasculature in multiple sclerosis by susceptibility-weighted imaging at 3.0 Tesla. J Magn Reson Imaging, 29(5), 1190-1194. doi:10.1002/jmri.21758
    25. Greenberg, S. M., Bacskai, B. J., Hernandez-Guillamon, M., Pruzin, J., Sperling, R., & van Veluw, S. J. (2020). Cerebral amyloid angiopathy and Alzheimer disease - one peptide, two pathways. Nat Rev Neurol, 16(1), 30-42. doi:10.1038/s41582-019-0281-2
    26. Haacke, E. M., Ge, Y., Sethi, S. K., Buch, S., & Zamboni, P. (2021). An Overview of Venous Abnormalities Related to the Development of Lesions in Multiple Sclerosis. Front Neurol, 12, 561458. doi:10.3389/fneur.2021.561458
    27. Haacke, E. M., Xu, Y., Cheng, Y. C., & Reichenbach, J. R. (2004). Susceptibility weighted imaging (SWI). Magn Reson Med, 52(3), 612-618. doi:10.1002/mrm.20198
    28. Hammond, K. E., Metcalf, M., Carvajal, L., Okuda, D. T., Srinivasan, R., Vigneron, D., . . . Pelletier, D. (2008). Quantitative in vivo magnetic resonance imaging of multiple sclerosis at 7 Tesla with sensitivity to iron. Ann Neurol, 64(6), 707-713. doi:10.1002/ana.21582
    29. Hartmann, D. A., Hyacinth, H. I., Liao, F. F., & Shih, A. Y. (2018). Does pathology of small venules contribute to cerebral microinfarcts and dementia? J Neurochem, 144(5), 517-526. doi:10.1111/jnc.14228
    30. Hooshmand, I., Rosenbaum, A. E., & Stein, R. L. (1974). Radiographic Anatomy of Normal Cerebral Deep Medullary Veins - Criteria for Distinguishing Them from Their Abnormal Counterparts. Neuroradiology, 7(2), 75-84. doi:Doi 10.1007/Bf00341874
    31. Iliff, J. J., Wang, M., Liao, Y., Plogg, B. A., Peng, W., Gundersen, G. A., . . . Nedergaard, M. (2012). A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med, 4(147), 147ra111. doi:10.1126/scitranslmed.3003748
    32. Jessen, N. A., Munk, A. S., Lundgaard, I., & Nedergaard, M. (2015). The Glymphatic System: A Beginner's Guide. Neurochem Res, 40(12), 2583-2599. doi:10.1007/s11064-015-1581-6
    33. Joo, I. L., Lai, A. Y., Bazzigaluppi, P., Koletar, M. M., Dorr, A., Brown, M. E., . . . Stefanovic, B. (2017). Early neurovascular dysfunction in a transgenic rat model of Alzheimer's disease. Sci Rep, 7, 46427. doi:10.1038/srep46427
    34. Kapadia, A., & Dmytriw, A. A. (2020). Multiple sclerosis is a systemic venous vasculopathy: A single unifying mechanism. Med Hypotheses, 140, 109645. doi:10.1016/j.mehy.2020.109645
    35. Karsdal, M. A., Nielsen, S. H., Leeming, D. J., Langholm, L. L., Nielsen, M. J., Manon-Jensen, T., . . . Schuppan, D. (2017). The good and the bad collagens of fibrosis - Their role in signaling and organ function. Adv Drug Deliv Rev, 121, 43-56. doi:10.1016/j.addr.2017.07.014
    36. Keith, J., Gao, F. Q., Noor, R., Kiss, A., Balasubramaniam, G., Au, K., . . . Black, S. E. (2017). Collagenosis of the Deep Medullary Veins: An Underrecognized Pathologic Correlate of White Matter Hyperintensities and Periventricular Infarction? J Neuropathol Exp Neurol, 76(4), 299-312. doi:10.1093/jnen/nlx009
    37. Khalatbari, H., Wright, J. N., Ishak, G. E., Perez, F. A., Amlie-Lefond, C. M., & Shaw, D. W. W. (2021). Deep medullary vein engorgement and superficial medullary vein engorgement: two patterns of perinatal venous stroke. Pediatr Radiol, 51(5), 675-685. doi:10.1007/s00247-020-04846-3
    38. Kilsdonk, I. D., Lopez-Soriano, A., Kuijer, J. P., de Graaf, W. L., Castelijns, J. A., Polman, C. H., . . . Wattjes, M. P. (2014). Morphological features of MS lesions on FLAIR* at 7 T and their relation to patient characteristics. J Neurol, 261(7), 1356-1364. doi:10.1007/s00415-014-7351-6
    39. Kilsdonk, I. D., Wattjes, M. P., Lopez-Soriano, A., Kuijer, J. P., de Jong, M. C., de Graaf, W. L., . . . Barkhof, F. (2014). Improved differentiation between MS and vascular brain lesions using FLAIR* at 7 Tesla. Eur Radiol, 24(4), 841-849. doi:10.1007/s00330-013-3080-y
    40. Kisling, A., Lust, R. M., & Katwa, L. C. (2019). What is the role of peptide fragments of collagen I and IV in health and disease? Life Sci, 228, 30-34. doi:10.1016/j.lfs.2019.04.042
    41. Kister, I., Herbert, J., Zhou, Y., & Ge, Y. (2013). Ultrahigh-Field MR (7 T) Imaging of Brain Lesions in Neuromyelitis Optica. Mult Scler Int, 2013, 398259. doi:10.1155/2013/398259
    42. Klakotskaia, D., Agca, C., Richardson, R. A., Stopa, E. G., Schachtman, T. R., & Agca, Y. (2018). Memory deficiency, cerebral amyloid angiopathy, and amyloid-beta plaques in APP+PS1 double transgenic rat model of Alzheimer's disease. PLoS One, 13(4), e0195469. doi:10.1371/journal.pone.0195469
    43. Kuchling, J., Ramien, C., Bozin, I., Dorr, J., Harms, L., Rosche, B., . . . Wuerfel, J. (2014). Identical lesion morphology in primary progressive and relapsing-remitting MS--an ultrahigh field MRI study. Mult Scler, 20(14), 1866-1871. doi:10.1177/1352458514531084
    44. Kuijf, H. J., Bouvy, W. H., Zwanenburg, J. J., Razoux Schultz, T. B., Viergever, M. A., Vincken, K. L., & Biessels, G. J. (2016). Quantification of deep medullary veins at 7 T brain MRI. Eur Radiol, 26(10), 3412-3418. doi:10.1007/s00330-016-4220-y
    45. Kulik, T., Kusano, Y., Aronhime, S., Sandler, A. L., & Winn, H. R. (2008). Regulation of cerebral vasculature in normal and ischemic brain. Neuropharmacology, 55(3), 281-288. doi:10.1016/j.neuropharm.2008.04.017
    46. Lahna, D., Schwartz, D. L., Woltjer, R., Black, S. E., Roese, N., Dodge, H., . . . Silbert, L. C. (2022). Venous Collagenosis as Pathogenesis of White Matter Hyperintensity. Ann Neurol. doi:10.1002/ana.26487
    47. Lin, J., Lan, L., Wang, D., Qiu, B., & Fan, Y. (2017). Cerebral Venous Collagen Remodeling in a Modified White Matter Lesions Animal Model. Neuroscience, 367, 72-84. doi:10.1016/j.neuroscience.2017.10.031
    48. Liu, Z. Y., Zhai, F. F., Ao, D. H., Han, F., Li, M. L., Zhou, L., . . . Zhu, Y. C. (2022). Deep medullary veins are associated with widespread brain structural abnormalities. J Cereb Blood Flow Metab, 42(6), 997-1006. doi:10.1177/0271678X211065210
    49. Mendel, T., Wierzba-Bobrowicz, T., Stepien, T., & Szpak, G. M. (2013). beta-amyloid deposits in veins in patients with cerebral amyloid angiopathy and intracerebral haemorrhage. Folia Neuropathol, 51(2), 120-126. doi:10.5114/fn.2013.35954
    50. Mistry, N., Abdel-Fahim, R., Samaraweera, A., Mougin, O., Tallantyre, E., Tench, C., . . . Evangelou, N. (2016). Imaging central veins in brain lesions with 3-T T2*-weighted magnetic resonance imaging differentiates multiple sclerosis from microangiopathic brain lesions. Mult Scler, 22(10), 1289-1296. doi:10.1177/1352458515616700
    51. Mistry, N., Dixon, J., Tallantyre, E., Tench, C., Abdel-Fahim, R., Jaspan, T., . . . Evangelou, N. (2013). Central veins in brain lesions visualized with high-field magnetic resonance imaging: a pathologically specific diagnostic biomarker for inflammatory demyelination in the brain. JAMA Neurol, 70(5), 623-628. doi:10.1001/jamaneurol.2013.1405
    52. Moody, D. M., Brown, W. R., Challa, V. R., & Anderson, R. L. (1995). Periventricular venous collagenosis: association with leukoaraiosis. Radiology, 194(2), 469-476. doi:10.1148/radiology.194.2.7824728
    53. Moody, D. M., Brown, W. R., Challa, V. R., GhaziBirry, H. S., & Reboussin, D. M. (1997). Cerebral microvascular alterations in aging, leukoaraiosis, and Alzheimer's disease. Cerebrovascular Pathology in Alzheimer's Disease, 826, 103-116. doi:DOI 10.1111/j.1749-6632.1997.tb48464.x
    54. Morrone, C. D., Bishay, J., & McLaurin, J. (2020). Potential Role of Venular Amyloid in Alzheimer's Disease Pathogenesis. Int J Mol Sci, 21(6). doi:10.3390/ijms21061985
    55. Okudera, T., Huang, Y. P., Fukusumi, A., Nakamura, Y., Hatazawa, J., & Uemura, K. (1999). Micro-angiographical studies of the medullary venous system of the cerebral hemisphere. Neuropathology, 19(1), 93-111. doi:10.1046/j.1440-1789.1999.00215.x
    56. Owens, T., Bechmann, I., & Engelhardt, B. (2008). Perivascular spaces and the two steps to neuroinflammation. J Neuropathol Exp Neurol, 67(12), 1113-1121. doi:10.1097/NEN.0b013e31818f9ca8
    57. Pantoni, L. (2010). Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol, 9(7), 689-701. doi:10.1016/S1474-4422(10)70104-6
    58. Pettersen, J. A., Keith, J., Gao, F., Spence, J. D., & Black, S. E. (2017). CADASIL accelerated by acute hypotension: Arterial and venous contribution to leukoaraiosis. Neurology, 88(11), 1077-1080. doi:10.1212/WNL.0000000000003717
    59. Poschl, E., Schlotzer-Schrehardt, U., Brachvogel, B., Saito, K., Ninomiya, Y., & Mayer, U. (2004). Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development, 131(7), 1619-1628. doi:10.1242/dev.01037
    60. Rae-Grant, A. D., Wong, C., Bernatowicz, R., & Fox, R. J. (2014). Observations on the brain vasculature in multiple sclerosis: A historical perspective. Mult Scler Relat Disord, 3(2), 156-162. doi:10.1016/j.msard.2013.08.005
    61. Reichenbach, J. R., Venkatesan, R., Schillinger, D. J., Kido, D. K., & Haacke, E. M. (1997). Small vessels in the human brain: MR venography with deoxyhemoglobin as an intrinsic contrast agent. Radiology, 204(1), 272-277. doi:10.1148/radiology.204.1.9205259
    62. Revesz, T., Ghiso, J., Lashley, T., Plant, G., Rostagno, A., Frangione, B., & Holton, J. L. (2003). Cerebral amyloid angiopathies: a pathologic, biochemical, and genetic view. J Neuropathol Exp Neurol, 62(9), 885-898. doi:10.1093/jnen/62.9.885
    63. Rhodin, J. A. (1968). Ultrastructure of mammalian venous capillaries, venules, and small collecting veins. J Ultrastruct Res, 25(5), 452-500. doi:10.1016/s0022-5320(68)80098-x
    64. Ringstad, G., Vatnehol, S. A. S., & Eide, P. K. (2017). Glymphatic MRI in idiopathic normal pressure hydrocephalus. Brain, 140(10), 2691-2705. doi:10.1093/brain/awx191
    65. Rivera-Rivera, L. A., Schubert, T., Turski, P., Johnson, K. M., Berman, S. E., Rowley, H. A., . . . Wieben, O. (2017). Changes in intracranial venous blood flow and pulsatility in Alzheimer's disease: A 4D flow MRI study. J Cereb Blood Flow Metab, 37(6), 2149-2158. doi:10.1177/0271678X16661340
    66. Roggendorf, W., & Cervos-Navarro, J. (1977). Ultrastructure of arterioles in the cat brain. Cell Tissue Res, 178(4), 495-515. doi:10.1007/BF00219571
    67. Roggendorf, W., Cervos-Navarro, J., & Lazaro-Lacalle, M. D. (1978). Ultrastructure of venules in the cat brain. Cell Tissue Res, 192(3), 461-474. doi:10.1007/BF00212326
    68. Sati, P., Oh, J., Constable, R. T., Evangelou, N., Guttmann, C. R., Henry, R. G., . . . Cooperative, N. (2016). The central vein sign and its clinical evaluation for the diagnosis of multiple sclerosis: a consensus statement from the North American Imaging in Multiple Sclerosis Cooperative. Nat Rev Neurol, 12(12), 714-722. doi:10.1038/nrneurol.2016.166
    69. Schmidek, H. H., Auer, L. M., & Kapp, J. P. (1985). The cerebral venous system. Neurosurgery, 17(4), 663-678. doi:10.1227/00006123-198510000-00024
    70. Shaaban, C. E., Aizenstein, H. J., Jorgensen, D. R., MacCloud, R. L., Meckes, N. A., Erickson, K. I., . . . Group, L. S. (2017). In Vivo Imaging of Venous Side Cerebral Small-Vessel Disease in Older Adults: An MRI Method at 7T. AJNR Am J Neuroradiol, 38(10), 1923-1928. doi:10.3174/ajnr.A5327
    71. Shen, Z., Lu, Z., Chhatbar, P. Y., O'Herron, P., & Kara, P. (2012). An artery-specific fluorescent dye for studying neurovascular coupling. Nat Methods, 9(3), 273-276. doi:10.1038/nmeth.1857
    72. Shi, H., Koronyo, Y., Rentsendorj, A., Fuchs, D. T., Sheyn, J., Black, K. L., . . . Koronyo-Hamaoui, M. (2021). Retinal Vasculopathy in Alzheimer's Disease. Front Neurosci, 15, 731614. doi:10.3389/fnins.2021.731614
    73. Shi, Y., Thrippleton, M. J., Blair, G. W., Dickie, D. A., Marshall, I., Hamilton, I., . . . Wardlaw, J. M. (2020). Small vessel disease is associated with altered cerebrovascular pulsatility but not resting cerebral blood flow. J Cereb Blood Flow Metab, 40(1), 85-99. doi:10.1177/0271678X18803956
    74. Sinnecker, T., Bozin, I., Dorr, J., Pfueller, C. F., Harms, L., Niendorf, T., . . . Wuerfel, J. (2013). Periventricular venous density in multiple sclerosis is inversely associated with T2 lesion count: a 7 Tesla MRI study. Mult Scler, 19(3), 316-325. doi:10.1177/1352458512451941
    75. Sinnecker, T., Dorr, J., Pfueller, C. F., Harms, L., Ruprecht, K., Jarius, S., . . . Paul, F. (2012). Distinct lesion morphology at 7-T MRI differentiates neuromyelitis optica from multiple sclerosis. Neurology, 79(7), 708-714. doi:10.1212/WNL.0b013e3182648bc8
    76. Staals, J., Booth, T., Morris, Z., Bastin, M. E., Gow, A. J., Corley, J., . . . Wardlaw, J. M. (2015). Total MRI load of cerebral small vessel disease and cognitive ability in older people. Neurobiol Aging, 36(10), 2806-2811. doi:10.1016/j.neurobiolaging.2015.06.024
    77. Takahashi, A., Ushiki, T., Abe, K., Houkin, K., & Abe, H. (1994). Cytoarchitecture of periendothelial cells in human cerebral venous vessels as compared with the scalp vein. A scanning electron microscopic study. Arch Histol Cytol, 57(4), 331-339. doi:10.1679/aohc.57.331
    78. Tallantyre, E. C., Brookes, M. J., Dixon, J. E., Morgan, P. S., Evangelou, N., & Morris, P. G. (2008). Demonstrating the perivascular distribution of MS lesions in vivo with 7-Tesla MRI. Neurology, 70(22), 2076-2078. doi:10.1212/01.wnl.0000313377.49555.2e
    79. Tan, I. L., van Schijndel, R. A., Pouwels, P. J., van Walderveen, M. A., Reichenbach, J. R., Manoliu, R. A., & Barkhof, F. (2000). MR venography of multiple sclerosis. AJNR Am J Neuroradiol, 21(6), 1039-1042. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/10871010
    80. Tanaka, R., Iwasaki, Y., & Koprowski, H. (1975). Ultrastructural studies of perivascular cuffing cells in multiple sclerosis brain. Am J Pathol, 81(3), 467-478. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/1211421
    81. Tang, V. W. (2020). Collagen, stiffness, and adhesion: the evolutionary basis of vertebrate mechanobiology. Mol Biol Cell, 31(17), 1823-1834. doi:10.1091/mbc.E19-12-0709
    82. Taoka, T., Fukusumi, A., Miyasaka, T., Kawai, H., Nakane, T., Kichikawa, K., & Naganawa, S. (2017). Structure of the Medullary Veins of the Cerebral Hemisphere and Related Disorders. Radiographics, 37(1), 281-297. doi:10.1148/rg.2017160061
    83. Ter Telgte, A., van Leijsen, E. M. C., Wiegertjes, K., Klijn, C. J. M., Tuladhar, A. M., & de Leeuw, F. E. (2018). Cerebral small vessel disease: from a focal to a global perspective. Nat Rev Neurol, 14(7), 387-398. doi:10.1038/s41582-018-0014-y
    84. Thal, D. R., Ghebremedhin, E., Rub, U., Yamaguchi, H., Del Tredici, K., & Braak, H. (2002). Two types of sporadic cerebral amyloid angiopathy. J Neuropathol Exp Neurol, 61(3), 282-293. doi:10.1093/jnen/61.3.282
    85. Uddin, M. A., Haq, T. U., & Rafique, M. Z. (2006). Cerebral venous system anatomy. J Pak Med Assoc, 56(11), 516-519. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/17183980
    86. Vanlandewijck, M., He, L., Mae, M. A., Andrae, J., Ando, K., Del Gaudio, F., . . . Betsholtz, C. (2018). A molecular atlas of cell types and zonation in the brain vasculature. Nature, 554(7693), 475-480. doi:10.1038/nature25739
    87. Weller, R. O., Boche, D., & Nicoll, J. A. (2009). Microvasculature changes and cerebral amyloid angiopathy in Alzheimer's disease and their potential impact on therapy. Acta Neuropathol, 118(1), 87-102. doi:10.1007/s00401-009-0498-z
    88. Weller, R. O., Massey, A., Newman, T. A., Hutchings, M., Kuo, Y. M., & Roher, A. E. (1998). Cerebral amyloid angiopathy: amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer's disease. Am J Pathol, 153(3), 725-733. doi:10.1016/s0002-9440(10)65616-7
    89. Whittaker, E., Thrippleton, S., Chong, L. Y. W., Collins, V. G., Ferguson, A. C., Henshall, D. E., . . . Rannikmae, K. (2022). Systematic Review of Cerebral Phenotypes Associated With Monogenic Cerebral Small-Vessel Disease. J Am Heart Assoc, 11(12), e025629. doi:10.1161/JAHA.121.025629
    90. Xu, Z., Li, F., Wang, B., Xing, D., Pei, Y., Yang, B., & Duan, Y. (2020). New Insights in Addressing Cerebral Small Vessel Disease: Association With the Deep Medullary Veins. Front Aging Neurosci, 12, 597799. doi:10.3389/fnagi.2020.597799
    91. Yan, S., Wan, J., Zhang, X., Tong, L., Zhao, S., Sun, J., . . . Lou, M. (2014). Increased visibility of deep medullary veins in leukoaraiosis: a 3-T MRI study. Front Aging Neurosci, 6, 144. doi:10.3389/fnagi.2014.00144
    92. Zeng, C., Chen, X., Li, Y., Ouyang, Y., Lv, F., Rumzan, R., & Wang, Z. (2013). Cerebral vein changes in relapsing-remitting multiple sclerosis demonstrated by three-dimensional enhanced T(2)-weighted angiography at 3.0 T. Eur Radiol, 23(3), 869-878. doi:10.1007/s00330-012-2637-5
    93. Zhang, K., Zhou, Y., Zhang, W., Li, Q., Sun, J., & Lou, M. (2022). MRI-visible perivascular spaces in basal ganglia but not centrum semiovale or hippocampus were related to deep medullary veins changes. J Cereb Blood Flow Metab, 42(1), 136-144. doi:10.1177/0271678X211038138
    94. Zhang, R., Huang, P., Jiaerken, Y., Wang, S., Hong, H., Luo, X., . . . Zhang, M. (2021). Venous disruption affects white matter integrity through increased interstitial fluid in cerebral small vessel disease. J Cereb Blood Flow Metab, 41(1), 157-165. doi:10.1177/0271678X20904840
    95. Zhang, R., Li, Q., Zhou, Y., Yan, S., Zhang, M., & Lou, M. (2019). The relationship between deep medullary veins score and the severity and distribution of intracranial microbleeds. Neuroimage Clin, 23, 101830. doi:10.1016/j.nicl.2019.101830
    96. Zhang, R., Zhou, Y., Yan, S., Zhong, G., Liu, C., Jiaerken, Y., . . . Lou, M. (2017). A Brain Region-Based Deep Medullary Veins Visual Score on Susceptibility Weighted Imaging. Front Aging Neurosci, 9, 269. doi:10.3389/fnagi.2017.00269
    97. Zhou, M., Mao, L., Wang, Y., Wang, Q., Yang, Z., Li, S., & Li, L. (2015). Morphologic changes of cerebral veins in hypertensive rats: venous collagenosis is associated with hypertension. J Stroke Cerebrovasc Dis, 24(3), 530-536. doi:10.1016/j.jstrokecerebrovasdis.2014.09.038
    98. Zhou, Y., Li, Q., Zhang, R., Zhang, W., Yan, S., Xu, J., . . . Lou, M. (2020). Role of deep medullary veins in pathogenesis of lacunes: Longitudinal observations from the CIRCLE study. J Cereb Blood Flow Metab, 40(9), 1797-1805. doi:10.1177/0271678X19882918

    How to Cite

    Wang, Pei, et al. “An Overview of Cerebral Venules: From Structure, Pathology, and Imaging to Related Diseases”. Human Brain, vol. 2, no. 1, Mar. 2023, doi:10.37819/hb.1.308.
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    DOI: https://doi.org/10.37819/hb.1.308

    Published: 2023-03-10

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