Barkhof F, Fox NC, Bastos-Leite AJ, Scheltens P (2011) Normal ageing. In: Neuroimaging in dementia. Springer, pp 43–57. https://doi.org/10.1007/978-3-642-00818-4_4
Rennels ML, Gregory TF, Blaumanis OR, Fujimoto K, Grady PA (1985) Evidence for a ‘paravascular’ fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space. Brain Res 326(1):47–63. https://doi.org/10.1016/0006-8993(85)91383-6
Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, 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. https://doi.org/10.1126/scitranslmed.3003748
Diem AK, MacGregor Sharp M, Gatherer M, Bressloff NW, Carare RO, Richardson G (2017) Arterial pulsations cannot drive intramural periarterial drainage: significance for Abeta drainage. Front Neurosci 11:475. https://doi.org/10.3389/fnins.2017.00475
Article
PubMed
PubMed Central
Google Scholar
Aspelund A, Antila S, Proulx ST, Karlsen TV, Karaman S, Detmar M, Wiig H, Alitalo K (2015) A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med 212(7):991–999. https://doi.org/10.1084/jem.20142290
CAS
Article
PubMed
PubMed Central
Google Scholar
Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, Derecki NC, Castle D, Mandell JW, Lee KS, Harris TH, Kipnis J (2015) Structural and functional features of central nervous system lymphatic vessels. Nature 523(7560):337–341. https://doi.org/10.1038/nature14432
CAS
Article
PubMed
PubMed Central
Google Scholar
Sun BL, Wang LH, Yang T, Sun JY, Mao LL, Yang MF, Yuan H, Colvin RA, Yang XY (2018) Lymphatic drainage system of the brain: a novel target for intervention of neurological diseases. Prog Neurobiol 163–164:118–143. https://doi.org/10.1016/j.pneurobio.2017.08.007
Article
PubMed
Google Scholar
Braffman BH, Zimmerman RA, Trojanowski JQ, Gonatas NK, Hickey WF, Schlaepfer WW (1988) Brain MR: pathologic correlation with gross and histopathology. 1. Lacunar infarction and Virchow-Robin spaces. AJR Am J Roentgenol 151 (3):551–558. https://doi.org/10.2214/ajr.151.3.551
Groeschel S, Chong WK, Surtees R, Hanefeld F (2006) Virchow-Robin spaces on magnetic resonance images: normative data, their dilatation, and a review of the literature. Neuroradiology 48(10):745–754. https://doi.org/10.1007/s00234-006-0112-1
Article
PubMed
Google Scholar
Woollam DH, Millen JW (1955) The perivascular spaces of the mammalian central nervous system and their relation to the perineuronal and subarachnoid spaces. J Anat 89(2):193–200
CAS
PubMed
PubMed Central
Google Scholar
Weed LH (1923) The absorption of cerebrospinal fluid into the venous system. Am J Anatomy 31(3):191–221. https://doi.org/10.1002/aja.1000310302
CAS
Article
Google Scholar
Krahn V (1982) The pia mater at the site of the entry of blood vessels into the central nervous system. Anat Embryol (Berl) 164(2):257–263. https://doi.org/10.1007/BF00318509
Zhang ET, Inman CB, Weller RO (1990) Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J Anat 170:111–123
Pollock H, Hutchings M, Weller RO, Zhang ET (1997) Perivascular spaces in the basal ganglia of the human brain: their relationship to lacunes. J Anat 191(Pt 3):337–346. https://doi.org/10.1046/j.1469-7580.1997.19130337.x
Morris AW, Sharp MM, Albargothy NJ, Fernandes R, Hawkes CA, Verma A, Weller RO, Carare RO (2016) Vascular basement membranes as pathways for the passage of fluid into and out of the brain. Acta Neuropathol 131(5):725–736. https://doi.org/10.1007/s00401-016-1555-z
CAS
Article
PubMed
PubMed Central
Google Scholar
Weller RO, Sharp MM, Christodoulides M, Carare RO, Mollgard K (2018) The meninges as barriers and facilitators for the movement of fluid, cells and pathogens related to the rodent and human CNS. Acta Neuropathol 135(3):363–385. https://doi.org/10.1007/s00401-018-1809-z
CAS
Article
PubMed
Google Scholar
Pizzo ME, Wolak DJ, Kumar NN, Brunette E, Brunnquell CL, Hannocks MJ, Abbott NJ, Meyerand ME, Sorokin L, Stanimirovic DB, Thorne RG (2018) Intrathecal antibody distribution in the rat brain: surface diffusion, perivascular transport and osmotic enhancement of delivery. J Physiol 596(3):445–475. https://doi.org/10.1113/JP275105
CAS
Article
PubMed
Google Scholar
Abbott NJ, Pizzo ME, Preston JE, Janigro D, Thorne RG (2018) The role of brain barriers in fluid movement in the CNS: is there a ‘glymphatic’ system? Acta Neuropathol 135(3):387–407. https://doi.org/10.1007/s00401-018-1812-4
CAS
Article
PubMed
Google Scholar
Zlokovic BV (2011) Neurovascular pathways to neurodegeneration in Alzheimer’s disease and other disorders. Nat Rev Neurosci 12(12):723–738. https://doi.org/10.1038/nrn3114
CAS
Article
PubMed
PubMed Central
Google Scholar
Cserr HF, Ostrach LH (1974) Bulk flow of interstitial fluid after intracranial injection of blue dextran 2000. Exp Neurol 45(1):50–60. https://doi.org/10.1016/0014-4886(74)90099-5
Iliff JJ, Wang M, Zeppenfeld DM, Venkataraman A, Plog BA, Liao Y, Deane R, Nedergaard M (2013) Cerebral arterial pulsation drives paravascular CSF-interstitial fluid exchange in the murine brain. J Neurosci 33(46):18190–18199. https://doi.org/10.1523/JNEUROSCI.1592-13.2013
CAS
Article
PubMed
PubMed Central
Google Scholar
Wolak DJ, Thorne RG (2013) Diffusion of macromolecules in the brain: implications for drug delivery. Mol Pharm 10(5):1492–1504. https://doi.org/10.1021/mp300495e
CAS
Article
PubMed
PubMed Central
Google Scholar
Smith AJ, Jin BJ, Verkman AS (2015) Muddying the water in brain edema? Trends Neurosci 38(6):331–332. https://doi.org/10.1016/j.tins.2015.04.006
CAS
Article
PubMed
PubMed Central
Google Scholar
Asgari M, de Zelicourt D, Kurtcuoglu V (2016) Glymphatic solute transport does not require bulk flow. Sci Rep 6:38635. https://doi.org/10.1038/srep38635
CAS
Article
PubMed
PubMed Central
Google Scholar
Smith AJ, Yao X, Dix JA, Jin BJ, Verkman AS (2017) Test of the ‘glymphatic’ hypothesis demonstrates diffusive and aquaporin-4-independent solute transport in rodent brain parenchyma. eLife 6. https://doi.org/10.7554/eLife.27679
Weller RO, Kida S, Zhang ET (1992) Pathways of fluid drainage from the brain–morphological aspects and immunological significance in rat and man. Brain Pathol 2(4):277–284. https://doi.org/10.1111/j.1750-3639.1992.tb00704.x
Preston SD, Steart PV, Wilkinson A, Nicoll JA, Weller RO (2003) Capillary and arterial cerebral amyloid angiopathy in Alzheimer’s disease: defining the perivascular route for the elimination of amyloid beta from the human brain. Neuropathol Appl Neurobiol 29(2):106–117. https://doi.org/10.1046/j.1365-2990.2003.00424.x
Weller RO, Nicoll JA (2003) Cerebral amyloid angiopathy: pathogenesis and effects on the ageing and Alzheimer brain. Neurol Res 25(6):611–616. https://doi.org/10.1179/016164103101202057
Article
PubMed
Google Scholar
Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JA, Perry VH, Weller RO (2008) Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol Appl Neurobiol 34(2):131–144. https://doi.org/10.1111/j.1365-2990.2007.00926.x
CAS
Article
PubMed
Google Scholar
Bakker EN, Bacskai BJ, Arbel-Ornath M, Aldea R, Bedussi B, Morris AW, Weller RO, Carare RO (2016) Lymphatic clearance of the brain: perivascular, paravascular and significance for neurodegenerative diseases. Cell Mol Neurobiol 36(2):181–194. https://doi.org/10.1007/s10571-015-0273-8
CAS
Article
PubMed
PubMed Central
Google Scholar
Schley D, Carare-Nnadi R, Please CP, Perry VH, Weller RO (2006) Mechanisms to explain the reverse perivascular transport of solutes out of the brain. J Theor Biol 238(4):962–974. https://doi.org/10.1016/j.jtbi.2005.07.005
CAS
Article
PubMed
Google Scholar
Di Marco LY, Farkas E, Martin C, Venneri A, Frangi AF (2015) Is vasomotion in cerebral arteries impaired in Alzheimer’s disease? J Alzheimers Dis 46(1):35–53. https://doi.org/10.3233/JAD-142976
CAS
Article
PubMed
PubMed Central
Google Scholar
Albargothy NJ, Johnston DA, MacGregor-Sharp M, Weller RO, Verma A, Hawkes CA, Carare RO (2018) Convective influx/glymphatic system: tracers injected into the CSF enter and leave the brain along separate periarterial basement membrane pathways. Acta Neuropathol. https://doi.org/10.1007/s00401-018-1862-7
Article
PubMed
PubMed Central
Google Scholar
Jayadev R, Sherwood DR (2017) Basement membranes. Curr Biol 27(6):R207–R211. https://doi.org/10.1016/j.cub.2017.02.006
CAS
Article
PubMed
Google Scholar
Bower NI, Hogan BM (2018) Brain drains: new insights into brain clearance pathways from lymphatic biology. J Mol Med (Berl) 96(5):383–390. https://doi.org/10.1007/s00109-018-1634-9
Article
Google Scholar
Shibata M, Yamada S, Kumar SR, Calero M, Bading J, Frangione B, Holtzman DM, Miller CA, Strickland DK, Ghiso J, Zlokovic BV (2000) Clearance of Alzheimer’s amyloid-beta1-40 peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J Clin Invest 106(12):1489–1499. https://doi.org/10.1172/JCI10498
CAS
Article
PubMed
PubMed Central
Google Scholar
Montagne A, Zhao Z, Zlokovic BV (2017) Alzheimer’s disease: a matter of blood-brain barrier dysfunction? J Exp Med 214(11):3151–3169. https://doi.org/10.1084/jem.20171406
CAS
Article
PubMed
PubMed Central
Google Scholar
Perry VH, Teeling J (2013) Microglia and macrophages of the central nervous system: the contribution of microglia priming and systemic inflammation to chronic neurodegeneration. Semin Immunopathol 35(5):601–612. https://doi.org/10.1007/s00281-013-0382-8
CAS
Article
PubMed
PubMed Central
Google Scholar
Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330(6005):841–845. https://doi.org/10.1126/science.1194637
CAS
Article
PubMed
PubMed Central
Google Scholar
London A, Cohen M, Schwartz M (2013) Microglia and monocyte-derived macrophages: functionally distinct populations that act in concert in CNS plasticity and repair. Front Cell Neurosci 7:34. https://doi.org/10.3389/fncel.2013.00034
CAS
Article
PubMed
PubMed Central
Google Scholar
Ma Q, Zhao Z, Sagare AP, Wu Y, Wang M, Owens NC, Verghese PB, Herz J, Holtzman DM, Zlokovic BV (2018) Blood-brain barrier-associated pericytes internalize and clear aggregated amyloid-beta42 by LRP1-dependent apolipoprotein E isoform-specific mechanism. Mol Neurodegener 13(1):57. https://doi.org/10.1186/s13024-018-0286-0
CAS
Article
PubMed
PubMed Central
Google Scholar
Mato M, Ookawara S (1981) Influences of age and vasopressin on the uptake capacity of fluorescent granular perithelial cells (FGP) of small cerebral vessels of the rat. Am J Anat 162(1):45–53. https://doi.org/10.1002/aja.1001620105
CAS
Article
PubMed
Google Scholar
van Lessen M, Shibata-Germanos S, van Impel A, Hawkins TA, Rihel J, Schulte-Merker S (2017) Intracellular uptake of macromolecules by brain lymphatic endothelial cells during zebrafish embryonic development. eLife 6. https://doi.org/10.7554/eLife.25932
Venero Galanternik M, Castranova D, Gore AV, Blewett NH, Jung HM, Stratman AN, Kirby MR, Iben J, Miller MF, Kawakami K, Maraia RJ, Weinstein BM (2017) A novel perivascular cell population in the zebrafish brain. eLife 6. https://doi.org/10.7554/eLife.24369
Tarasoff-Conway JM, Carare RO, Osorio RS, Glodzik L, Butler T, Fieremans E, Axel L, Rusinek H, Nicholson C, Zlokovic BV, Frangione B, Blennow K, Menard J, Zetterberg H, Wisniewski T, de Leon MJ (2015) Clearance systems in the brain-implications for Alzheimer disease. Nat Rev Neurol 11(8):457–470. https://doi.org/10.1038/nrneurol.2015.119
CAS
Article
PubMed
PubMed Central
Google Scholar
Johanson CE, Duncan JA 3rd, Klinge PM, Brinker T, Stopa EG, Silverberg GD (2008) Multiplicity of cerebrospinal fluid functions: new challenges in health and disease. Cerebrospinal Fluid Res 5:10. https://doi.org/10.1186/1743-8454-5-10
CAS
Article
PubMed
PubMed Central
Google Scholar
Oreskovic D, Klarica M (2010) The formation of cerebrospinal fluid: nearly a hundred years of interpretations and misinterpretations. Brain Res Rev 64(2):241–262. https://doi.org/10.1016/j.brainresrev.2010.04.006
CAS
Article
PubMed
Google Scholar
Bulat M, Klarica M (2011) Recent insights into a new hydrodynamics of the cerebrospinal fluid. Brain Res Rev 65(2):99–112. https://doi.org/10.1016/j.brainresrev.2010.08.002
Article
PubMed
Google Scholar
Oreskovic D, Rados M, Klarica M (2017) Role of choroid plexus in cerebrospinal fluid hydrodynamics. Neuroscience 354:69–87. https://doi.org/10.1016/j.neuroscience.2017.04.025
CAS
Article
PubMed
Google Scholar
Bradbury MW, Cserr HF, Westrop RJ (1981) Drainage of cerebral interstitial fluid into deep cervical lymph of the rabbit. Am J Physiol 240(4):F329-336. https://doi.org/10.1152/ajprenal.1981.240.4.F329
CAS
Article
PubMed
Google Scholar
Szentistvanyi I, Patlak CS, Ellis RA, Cserr HF (1984) Drainage of interstitial fluid from different regions of rat brain. Am J Physiol 246(6 Pt 2):F835-844. https://doi.org/10.1152/ajprenal.1984.246.6.F835
CAS
Article
PubMed
Google Scholar
Engelhardt B, Carare RO, Bechmann I, Flugel A, Laman JD, Weller RO (2016) Vascular, glial, and lymphatic immune gateways of the central nervous system. Acta Neuropathol 132(3):317–338. https://doi.org/10.1007/s00401-016-1606-5
CAS
Article
PubMed
PubMed Central
Google Scholar
Absinta M, Ha SK, Nair G, Sati P, Luciano NJ, Palisoc M, Louveau A, Zaghloul KA, Pittaluga S, Kipnis J, Reich DS (2017) Human and nonhuman primate meninges harbor lymphatic vessels that can be visualized noninvasively by MRI. eLife 6. https://doi.org/10.7554/eLife.29738
Raper D, Louveau A, Kipnis J (2016) How do meningeal lymphatic vessels drain the CNS? Trends Neurosci 39(9):581–586. https://doi.org/10.1016/j.tins.2016.07.001
CAS
Article
PubMed
PubMed Central
Google Scholar
Da Mesquita S, Louveau A, Vaccari A, Smirnov I, Cornelison RC, Kingsmore KM, Contarino C, Onengut-Gumuscu S, Farber E, Raper D, Viar KE, Powell RD, Baker W, Dabhi N, Bai R, Cao R, Hu S, Rich SS, Munson JM, Lopes MB, Overall CC, Acton ST, Kipnis J (2018) Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease. Nature 560(7717):185–191. https://doi.org/10.1038/s41586-018-0368-8
CAS
Article
PubMed
PubMed Central
Google Scholar
Weller RO, Subash M, Preston SD, Mazanti I, Carare RO (2008) Perivascular drainage of amyloid-beta peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer’s disease. Brain Pathol 18(2):253–266. https://doi.org/10.1111/j.1750-3639.2008.00133.x
CAS
Article
PubMed
Google Scholar
Fonck E, Feigl GG, Fasel J, Sage D, Unser M, Rufenacht DA, Stergiopulos N (2009) Effect of aging on elastin functionality in human cerebral arteries. Stroke 40(7):2552–2556. https://doi.org/10.1161/STROKEAHA.108.528091
CAS
Article
PubMed
Google Scholar
Weller RO, Djuanda E, Yow HY, Carare RO (2009) Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol 117(1):1–14. https://doi.org/10.1007/s00401-008-0457-0
CAS
Article
PubMed
Google Scholar
Farkas E, de Vos RA, Donka G, Jansen Steur EN, Mihaly A, Luiten PG (2006) Age-related microvascular degeneration in the human cerebral periventricular white matter. Acta Neuropathol 111(2):150–157. https://doi.org/10.1007/s00401-005-0007-y
Article
PubMed
Google Scholar
Alamowitch S, Plaisier E, Favrole P, Prost C, Chen Z, Van Agtmael T, Marro B, Ronco P (2009) Cerebrovascular disease related to COL4A1 mutations in HANAC syndrome. Neurology 73(22):1873–1882. https://doi.org/10.1212/WNL.0b013e3181c3fd12
CAS
Article
PubMed
PubMed Central
Google Scholar
Lanfranconi S, Markus HS (2010) COL4A1 mutations as a monogenic cause of cerebral small vessel disease: a systematic review. Stroke 41(8):e513-518. https://doi.org/10.1161/STROKEAHA.110.581918
Article
PubMed
Google Scholar
Mestre H, Kostrikov S, Mehta RI, Nedergaard M (2017) Perivascular spaces, glymphatic dysfunction, and small vessel disease. Clin Sci (Lond) 131(17):2257–2274. https://doi.org/10.1042/CS20160381
CAS
Article
Google Scholar
Hawkes CA, Gentleman SM, Nicoll JA, Carare RO (2015) Prenatal high-fat diet alters the cerebrovasculature and clearance of beta-amyloid in adult offspring. J Pathol 235(4):619–631. https://doi.org/10.1002/path.4468
CAS
Article
PubMed
Google Scholar
Sweeney MD, Zhao Z, Montagne A, Nelson AR, Zlokovic BV (2019) Blood-brain barrier: from physiology to disease and back. Physiol Rev 99(1):21–78. https://doi.org/10.1152/physrev.00050.2017
CAS
Article
PubMed
Google Scholar
Bowman GL, Dayon L, Kirkland R, Wojcik J, Peyratout G, Severin IC, Henry H, Oikonomidi A, Migliavacca E, Bacher M, Popp J (2018) Blood-brain barrier breakdown, neuroinflammation, and cognitive decline in older adults. Alzheimers Dement 14(12):1640–1650. https://doi.org/10.1016/j.jalz.2018.06.2857
Article
PubMed
Google Scholar
Kress BT, Iliff JJ, Xia M, Wang M, Wei HS, Zeppenfeld D, Xie L, Kang H, Xu Q, Liew JA, Plog BA, Ding F, Deane R, Nedergaard M (2014) Impairment of paravascular clearance pathways in the aging brain. Ann Neurol 76(6):845–861. https://doi.org/10.1002/ana.24271
CAS
Article
PubMed
PubMed Central
Google Scholar
Barkhof F, Fox NC, Bastos-Leite AJ, Scheltens P (2011) Neuroimaging in dementia. Springer. https://doi.org/10.1007/978-3-642-00818-4
Article
Google Scholar
Bastos Leite AJ, Scheltens P, Barkhof F (2004) Pathological aging of the brain: an overview. Top Magn Reson Imaging 15(6):369–389. https://doi.org/10.1097/01.rmr.0000168070.90113.dc
Article
PubMed
Google Scholar
Bastos-Leite AJ, van der Flier WM, van Straaten EC, Staekenborg SS, Scheltens P, Barkhof F (2007) The contribution of medial temporal lobe atrophy and vascular pathology to cognitive impairment in vascular dementia. Stroke 38(12):3182–3185. https://doi.org/10.1161/STROKEAHA.107.490102
Article
PubMed
Google Scholar
Ramirez J, Berezuk C, McNeely AA, Gao F, McLaurin J, Black SE (2016) Imaging the perivascular space as a potential biomarker of neurovascular and neurodegenerative diseases. Cell Mol Neurobiol 36(2):289–299. https://doi.org/10.1007/s10571-016-0343-6
CAS
Article
PubMed
Google Scholar
Patankar TF, Mitra D, Varma A, Snowden J, Neary D, Jackson A (2005) Dilatation of the Virchow-Robin space is a sensitive indicator of cerebral microvascular disease: study in elderly patients with dementia. AJNR Am J Neuroradiol 26(6):1512–1520
PubMed
PubMed Central
Google Scholar
Potter GM, Doubal FN, Jackson CA, Chappell FM, Sudlow CL, Dennis MS, Wardlaw JM (2015) Enlarged perivascular spaces and cerebral small vessel disease. Int J Stroke 10(3):376–381. https://doi.org/10.1111/ijs.12054
Article
PubMed
Google Scholar
Bokura H, Kobayashi S, Yamaguchi S (1998) Distinguishing silent lacunar infarction from enlarged Virchow-Robin spaces: a magnetic resonance imaging and pathological study. J Neurol 245(2):116–122. https://doi.org/10.1007/s004150050189
Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O’Brien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, DeCarli C, de Leeuw FE, Doubal F, Duering M, Fox NC, Greenberg S, Hachinski V, Kilimann I, Mok V, Oostenbrugge R, Pantoni L, Speck O, Stephan BC, Teipel S, Viswanathan A, Werring D, Chen C, Smith C, van Buchem M, Norrving B, Gorelick PB, Dichgans M, STandards for ReportIng Vascular changes on nEuroimaging (STRIVE v1) (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12(8):822–838. https://doi.org/10.1016/S1474-4422(13)70124-8
Kwee RM, Kwee TC (2007) Virchow-Robin spaces at MR imaging. Radiographics 27(4):1071–1086. https://doi.org/10.1148/rg.274065722
Article
PubMed
Google Scholar
van der Knaap MS, Valk J (2005) Magnetic resonance of myelination and myelin disorders. Springer. https://doi.org/10.1007/3-540-27660-2
Article
Google Scholar
Adams HH, Hilal S, Schwingenschuh P, Wittfeld K, van der Lee SJ, DeCarli C, Vernooij MW, Katschnig-Winter P, Habes M, Chen C, Seshadri S, van Duijn CM, Ikram MK, Grabe HJ, Schmidt R, Ikram MA (2015) A priori collaboration in population imaging: the Uniform Neuro-Imaging of Virchow-Robin Spaces Enlargement consortium. Alzheimers Dement (Amst) 1(4):513–520. https://doi.org/10.1016/j.dadm.2015.10.004
Article
Google Scholar
Potter GM, Chappell FM, Morris Z, Wardlaw JM (2015) Cerebral perivascular spaces visible on magnetic resonance imaging: development of a qualitative rating scale and its observer reliability. Cerebrovasc Dis 39(3–4):224–231. https://doi.org/10.1159/000375153
Article
PubMed
PubMed Central
Google Scholar
Maclullich AM, Wardlaw JM, Ferguson KJ, Starr JM, Seckl JR, Deary IJ (2004) Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. J Neurol Neurosurg Psychiatry 75(11):1519–1523. https://doi.org/10.1136/jnnp.2003.030858
CAS
Article
PubMed
PubMed Central
Google Scholar
Ballerini L, Booth T, Valdes Hernandez MDC, Wiseman S, Lovreglio R, Munoz Maniega S, Morris Z, Pattie A, Corley J, Gow A, Bastin ME, Deary IJ, Wardlaw J (2020) Computational quantification of brain perivascular space morphologies: associations with vascular risk factors and white matter hyperintensities. A study in the Lothian Birth Cohort 1936. NeuroImage Clin 25:102120.https://doi.org/10.1016/j.nicl.2019.102120
Ramirez J, Berezuk C, McNeely AA, Scott CJ, Gao F, Black SE (2015) Visible Virchow-Robin spaces on magnetic resonance imaging of Alzheimer’s disease patients and normal elderly from the Sunnybrook Dementia Study. J Alzheimers Dis 43(2):415–424. https://doi.org/10.3233/JAD-132528
Article
PubMed
Google Scholar
Wang X, Valdes Hernandez Mdel C, Doubal F, Chappell FM, Piper RJ, Deary IJ, Wardlaw JM (2016) Development and initial evaluation of a semi-automatic approach to assess perivascular spaces on conventional magnetic resonance images. J Neurosci Methods 257:34–44. https://doi.org/10.1016/j.jneumeth.2015.09.010
Article
PubMed
PubMed Central
Google Scholar
Dubost F, Yilmaz P, Adams H, Bortsova G, Ikram MA, Niessen W, Vernooij M, de Bruijne M (2019) Enlarged perivascular spaces in brain MRI: automated quantification in four regions. NeuroImage 185:534–544. https://doi.org/10.1016/j.neuroimage.2018.10.026
Article
PubMed
Google Scholar
Ballerini L, Lovreglio R, Valdes Hernandez MDC, Ramirez J, MacIntosh BJ, Black SE, Wardlaw JM (2018) Perivascular spaces segmentation in brain MRI using optimal 3D filtering. Sci Rep 8(1):2132. https://doi.org/10.1038/s41598-018-19781-5
CAS
Article
PubMed
PubMed Central
Google Scholar
Sepehrband F, Barisano G, Sheikh-Bahaei N, Cabeen RP, Choupan J, Law M, Toga AW (2019) Image processing approaches to enhance perivascular space visibility and quantification using MRI. Sci Rep 9(1):12351. https://doi.org/10.1038/s41598-019-48910-x
CAS
Article
PubMed
PubMed Central
Google Scholar
Schwartz DL, Boespflug EL, Lahna DL, Pollock J, Roese NE, Silbert LC (2019) Autoidentification of perivascular spaces in white matter using clinical field strength T1 and FLAIR MR imaging. NeuroImage 202:116126. https://doi.org/10.1016/j.neuroimage.2019.116126
Article
PubMed
Google Scholar
Boespflug EL, Schwartz DL, Lahna D, Pollock J, Iliff JJ, Kaye JA, Rooney W, Silbert LC (2018) MR imaging-based multimodal autoidentification of perivascular spaces (mMAPS): automated morphologic segmentation of enlarged perivascular spaces at clinical field strength. Radiology 286(2):632–642. https://doi.org/10.1148/radiol.2017170205
Article
PubMed
Google Scholar
Eide PK, Ringstad G (2015) MRI with intrathecal MRI gadolinium contrast medium administration: a possible method to assess glymphatic function in human brain. Acta Radiol Open 4(11):2058460115609635. https://doi.org/10.1177/2058460115609635
Article
PubMed
PubMed Central
Google Scholar
Taoka T, Naganawa S (2020) Glymphatic imaging using MRI. J Magn Reson Imaging 51(1):11–24. https://doi.org/10.1002/jmri.26892
Article
PubMed
Google Scholar
Taoka T, Masutani Y, Kawai H, Nakane T, Matsuoka K, Yasuno F, Kishimoto T, Naganawa S (2017) Evaluation of glymphatic system activity with the diffusion MR technique: diffusion tensor image analysis along the perivascular space (DTI-ALPS) in Alzheimer’s disease cases. Jpn J Radiol 35(4):172–178. https://doi.org/10.1007/s11604-017-0617-z
Article
PubMed
Google Scholar
van Veluw SJ, Biessels GJ, Bouvy WH, Spliet WG, Zwanenburg JJ, Luijten PR, Macklin EA, Rozemuller AJ, Gurol ME, Greenberg SM, Viswanathan A, Martinez-Ramirez S (2016) Cerebral amyloid angiopathy severity is linked to dilation of juxtacortical perivascular spaces. J Cereb Blood Flow Metab 36(3):576–580. https://doi.org/10.1177/0271678X15620434
CAS
Article
PubMed
Google Scholar
Cai K, Tain R, Das S, Damen FC, Sui Y, Valyi-Nagy T, Elliott MA, Zhou XJ (2015) The feasibility of quantitative MRI of perivascular spaces at 7T. J Neurosci Methods 256:151–156. https://doi.org/10.1016/j.jneumeth.2015.09.001
Article
PubMed
PubMed Central
Google Scholar
Barisano G, Law M, Custer RM, Toga AW, Sepehrband F (2021) Perivascular space imaging at ultrahigh field MR imaging. Magn Reson Imaging Clin N Am 29(1):67–75. https://doi.org/10.1016/j.mric.2020.09.005
Article
PubMed
Google Scholar
Rajna Z, Raitamaa L, Tuovinen T, Heikkila J, Kiviniemi V, Seppanen T (2019) 3D multi-resolution optical flow analysis of cardiovascular pulse propagation in human brain. IEEE Trans Med Imaging 38(9):2028–2036. https://doi.org/10.1109/TMI.2019.2904762
Article
PubMed
Google Scholar
Barkhof F (2004) Enlarged Virchow-Robin spaces: do they matter? J Neurol Neurosurg Psychiatry 75(11):1516–1517. https://doi.org/10.1136/jnnp.2004.044578
CAS
Article
PubMed
PubMed Central
Google Scholar
Awad IA, Johnson PC, Spetzler RF, Hodak JA (1986) Incidental subcortical lesions identified on magnetic resonance imaging in the elderly. II Postmortem pathological correlations. Stroke 17(6):1090–1097. https://doi.org/10.1161/01.STR.17.6.1090
Erkinjuntti T, Inzitari D, Pantoni L, Wallin A, Scheltens P, Rockwood K, Roman GC, Chui H, Desmond DW (2000) Research criteria for subcortical vascular dementia in clinical trials. J Neural Transm Suppl 59:23–30. https://doi.org/10.1007/978-3-7091-6781-6_4
Bastos-Leite AJ, Kuijer JP, Rombouts SA, Sanz-Arigita E, van Straaten EC, Gouw AA, van der Flier WM, Scheltens P, Barkhof F (2008) Cerebral blood flow by using pulsed arterial spin-labeling in elderly subjects with white matter hyperintensities. AJNR Am J Neuroradiol 29(7):1296–1301. https://doi.org/10.3174/ajnr.A1091
CAS
Article
PubMed
PubMed Central
Google Scholar
Shams S, Martola J, Cavallin L, Granberg T, Shams M, Aspelin P, Wahlund LO, Kristoffersen-Wiberg M (2015) SWI or T2*: which MRI sequence to use in the detection of cerebral microbleeds? The Karolinska Imaging Dementia Study. AJNR Am J Neuroradiol 36(6):1089–1095. https://doi.org/10.3174/ajnr.A4248
CAS
Article
PubMed
PubMed Central
Google Scholar
Greenberg SM, Charidimou A (2018) Diagnosis of cerebral amyloid angiopathy: evolution of the Boston Criteria. Stroke 49(2):491–497. https://doi.org/10.1161/STROKEAHA.117.016990
Article
PubMed
PubMed Central
Google Scholar
Barkhof F, Fox NC, Bastos-Leite AJ, Scheltens P (2011) Vascular dementia. In: Neuroimaging in dementia. Springer, pp 137–176. https://doi.org/10.1007/978-3-642-00818-4_6
Ryan NS, Bastos-Leite AJ, Rohrer JD, Werring DJ, Fox NC, Rossor MN, Schott JM (2012) Cerebral microbleeds in familial Alzheimer’s disease. Brain 135 (Pt 1):e201; author reply e202. https://doi.org/10.1093/brain/awr126
Charidimou A, Boulouis G, Pasi M, Auriel E, van Etten ES, Haley K, Ayres A, Schwab KM, Martinez-Ramirez S, Goldstein JN, Rosand J, Viswanathan A, Greenberg SM, Gurol ME (2017) MRI-visible perivascular spaces in cerebral amyloid angiopathy and hypertensive arteriopathy. Neurology 88(12):1157–1164. https://doi.org/10.1212/WNL.0000000000003746
CAS
Article
PubMed
PubMed Central
Google Scholar
Saito S, Ihara M (2014) New therapeutic approaches for Alzheimer’s disease and cerebral amyloid angiopathy. Front Aging Neurosci 6:290. https://doi.org/10.3389/fnagi.2014.00290
Article
PubMed
PubMed Central
Google Scholar
Plog BA, Nedergaard M (2018) The glymphatic system in central nervous system health and disease: past, present, and future. Annu Rev Pathol 13:379–394. https://doi.org/10.1146/annurev-pathol-051217-111018
CAS
Article
PubMed
PubMed Central
Google Scholar
Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, O’Donnell J, Christensen DJ, Nicholson C, Iliff JJ, Takano T, Deane R, Nedergaard M (2013) Sleep drives metabolite clearance from the adult brain. Science 342(6156):373–377. https://doi.org/10.1126/science.1241224
CAS
Article
PubMed
Google Scholar
Shokri-Kojori E, Wang GJ, Wiers CE, Demiral SB, Guo M, Kim SW, Lindgren E, Ramirez V, Zehra A, Freeman C, Miller G, Manza P, Srivastava T, De Santi S, Tomasi D, Benveniste H, Volkow ND (2018) β-Amyloid accumulation in the human brain after one night of sleep deprivation. Proc Natl Acad Sci U S A 115(17):4483–4488. https://doi.org/10.1073/pnas.1721694115
CAS
Article
PubMed
PubMed Central
Google Scholar
Lucey BP, Bateman RJ (2014) Amyloid-beta diurnal pattern: possible role of sleep in Alzheimer’s disease pathogenesis. Neurobiol Aging 35(Suppl 2):S29-34. https://doi.org/10.1016/j.neurobiolaging.2014.03.035
CAS
Article
PubMed
Google Scholar
Lee H, Xie L, Yu M, Kang H, Feng T, Deane R, Logan J, Nedergaard M, Benveniste H (2015) The effect of body posture on brain glymphatic transport. J Neurosci 35(31):11034–11044. https://doi.org/10.1523/JNEUROSCI.1625-15.2015
CAS
Article
PubMed
PubMed Central
Google Scholar
Wu H, Mahmood A, Lu D, Jiang H, Xiong Y, Zhou D, Chopp M (2010) Attenuation of astrogliosis and modulation of endothelial growth factor receptor in lipid rafts by simvastatin after traumatic brain injury. J Neurosurg 113(3):591–597. https://doi.org/10.3171/2009.9.JNS09859
CAS
Article
PubMed
PubMed Central
Google Scholar
Iliff JJ, Chen MJ, Plog BA, Zeppenfeld DM, Soltero M, Yang L, Singh I, Deane R, Nedergaard M (2014) Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J Neurosci 34(49):16180–16193. https://doi.org/10.1523/JNEUROSCI.3020-14.2014
CAS
Article
PubMed
PubMed Central
Google Scholar
He XF, Liu DX, Zhang Q, Liang FY, Dai GY, Zeng JS, Pei Z, Xu GQ, Lan Y (2017) Voluntary exercise promotes glymphatic clearance of amyloid beta and reduces the activation of astrocytes and microglia in aged mice. Front Mol Neurosci 10:144. https://doi.org/10.3389/fnmol.2017.00144
CAS
Article
PubMed
PubMed Central
Google Scholar
Burgess A, Dubey S, Yeung S, Hough O, Eterman N, Aubert I, Hynynen K (2014) Alzheimer disease in a mouse model: MR imaging-guided focused ultrasound targeted to the hippocampus opens the blood-brain barrier and improves pathologic abnormalities and behavior. Radiology 273(3):736–745. https://doi.org/10.1148/radiol.14140245
Article
PubMed
Google Scholar
Leinenga G, Gotz J (2015) Scanning ultrasound removes amyloid-beta and restores memory in an Alzheimer’s disease mouse model. Sci Transl Med 7 (278):278ra233. https://doi.org/10.1126/scitranslmed.aaa2512
Hawkes CA, McLaurin J (2009) Selective targeting of perivascular macrophages for clearance of beta-amyloid in cerebral amyloid angiopathy. Proc Natl Acad Sci U S A 106(4):1261–1266. https://doi.org/10.1073/pnas.0805453106
Article
PubMed
PubMed Central
Google Scholar
Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Liao Z, Lieberburg I, Motter R, Mutter L, Soriano F, Shopp G, Vasquez N, Vandevert C, Walker S, Wogulis M, Yednock T, Games D, Seubert P (1999) Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400(6740):173–177. https://doi.org/10.1038/22124
CAS
Article
PubMed
Google Scholar
Check E (2002) Nerve inflammation halts trial for Alzheimer’s drug. Nature 415(6871):462. https://doi.org/10.1038/415462a
CAS
Article
PubMed
Google Scholar
Nicoll JA, Wilkinson D, Holmes C, Steart P, Markham H, Weller RO (2003) Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: a case report. Nat Med 9(4):448–452. https://doi.org/10.1038/nm840
CAS
Article
PubMed
Google Scholar
Patton RL, Kalback WM, Esh CL, Kokjohn TA, Van Vickle GD, Luehrs DC, Kuo YM, Lopez J, Brune D, Ferrer I, Masliah E, Newel AJ, Beach TG, Castano EM, Roher AE (2006) Amyloid-beta peptide remnants in AN-1792-immunized Alzheimer’s disease patients: a biochemical analysis. Am J Pathol 169(3):1048–1063
CAS
Article
PubMed
PubMed Central
Google Scholar
Carare RO (2017) Editorial: clearance pathways for amyloid-beta. Significance for Alzheimer’s disease and its therapy. Front Aging Neurosci 9:339. https://doi.org/10.3389/fnagi.2017.00339
Diem AK, Tan M, Bressloff NW, Hawkes C, Morris AW, Weller RO, Carare RO (2016) A simulation model of periarterial clearance of amyloid-beta from the brain. Front Aging Neurosci 8:18. https://doi.org/10.3389/fnagi.2016.00018
CAS
Article
PubMed
PubMed Central
Google Scholar
Braak H, Braak E, Bohl J, Reintjes R (1996) Age, neurofibrillary changes, Aβ-amyloid and the onset of Alzheimer’s disease. Neurosci Lett 210(2):87–90
CAS
Article
PubMed
Google Scholar