The glymphatic system's role in traumatic brain injury-related neurodegeneration.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
Jul 2023
Jul 2023
Historique:
received:
25
11
2022
accepted:
05
04
2023
revised:
03
04
2023
medline:
1
11
2023
pubmed:
15
5
2023
entrez:
15
5
2023
Statut:
ppublish
Résumé
In at least some individuals who suffer a traumatic brain injury (TBI), there exists a risk of future neurodegenerative illness. This review focuses on the association between the brain-based paravascular drainage pathway known as the "glymphatic system" and TBI-related neurodegeneration. The glymphatic system is composed of cerebrospinal fluid (CSF) flowing into the brain parenchyma along paravascular spaces surrounding penetrating arterioles where it mixes with interstitial fluid (ISF) before being cleared along paravenous drainage pathways. Aquaporin-4 (AQP4) water channels on astrocytic end-feet appear essential for the functioning of this system. The current literature linking glymphatic system disruption and TBI-related neurodegeneration is largely based on murine models with existing human research focused on the need for biomarkers of glymphatic system function (e.g., neuroimaging modalities). Key findings from the existing literature include evidence of glymphatic system flow disruption following TBI, mechanisms of this decreased flow (i.e., AQP4 depolarization), and evidence of protein accumulation and deposition (e.g., amyloid β, tau). The same studies suggest that glymphatic dysfunction leads to subsequent neurodegeneration, cognitive decline, and/or behavioral change although replication in humans is needed. Identified emerging topics from the literature are as follows: link between TBI, sleep, and glymphatic system dysfunction; influence of glymphatic system disruption on TBI biomarkers; and development of novel treatments for glymphatic system disruption following TBI. Although a burgeoning field, more research is needed to elucidate the role of glymphatic system disruption in TBI-related neurodegeneration.
Identifiants
pubmed: 37185960
doi: 10.1038/s41380-023-02070-7
pii: 10.1038/s41380-023-02070-7
doi:
Substances chimiques
Amyloid beta-Peptides
0
Aquaporin 4
0
Biomarkers
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2707-2715Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Martland HS. Punch drunk. J Am Med Assoc. 1928;91:1103–7.
Critchley M. Medical aspects of boxing, particularly from a neurological standpoint. Br Med J. 1957;1:357–62.
pubmed: 13396257
pmcid: 1974382
doi: 10.1136/bmj.1.5015.357
McKee AC, Cairns NJ, Dickson DW, Folkerth RD, Keene CD, Litvan I, et al. The first NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. Acta Neuropathol. 2016;131:75–86.
pubmed: 26667418
doi: 10.1007/s00401-015-1515-z
Bieniek KF, Cairns NJ, Crary JF, Dickson DW, Folkerth RD, Keene CD, et al. The second NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. J Neuropathol Exp Neurol. 2021;80:210–9.
pubmed: 33611507
pmcid: 7899277
Graham NS, Sharp DJ. Understanding neurodegeneration after traumatic brain injury: from mechanisms to clinical trials in dementia. J Neurol Neurosurg Psychiatry. 2019;90:1221–33.
pubmed: 31542723
doi: 10.1136/jnnp-2017-317557
LoBue C, Cullum CM, Didehbani N, Yeatman K, Jones B, Kraut MA, et al. Neurodegenerative dementias after traumatic brain injury. J Neuropsychiatry Clin Neurosci. 2018;30:7–13.
pubmed: 29061090
doi: 10.1176/appi.neuropsych.17070145
McAllister TW. Neurobiological consequences of traumatic brain injury. Dialogues Clin Neurosci. 2011;13:287–300.
pubmed: 22033563
pmcid: 3182015
doi: 10.31887/DCNS.2011.13.2/tmcallister
Washington PM, Villapol S, Burns MP. Polypathology and dementia after brain trauma: does brain injury trigger distinct neurodegenerative diseases, or should they be classified together as traumatic encephalopathy? Exp Neurol. 2016;275:381–8.
pubmed: 26091850
doi: 10.1016/j.expneurol.2015.06.015
Williamson MLC, Elliott TR, Bogner J, Dreer LE, Arango-Lasprilla JC, Kolakowsky-Hayner SA, et al. Trajectories of life satisfaction over the first 10 years after traumatic brain injury: race, gender, and functional ability. J Head Trauma Rehabil. 2016;31:167–79.
pubmed: 25699619
doi: 10.1097/HTR.0000000000000111
Juengst SB, Adams LM, Bogner JA, Arenth PM, O’Neil-Pirozzi TM, Dreer LE, et al. Trajectories of life satisfaction after traumatic brain injury: influence of life roles, age, cognitive disability, and depressive symptoms. Rehabil Psychol. 2015;60:353–64.
pubmed: 26618215
pmcid: 4667543
doi: 10.1037/rep0000056
Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med. 2012;4:147ra111.
pubmed: 22896675
pmcid: 3551275
doi: 10.1126/scitranslmed.3003748
Iliff JJ, Chen MJ, Plog BA, Zeppenfeld DM, Soltero M, Yang L, et al. Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J Neurosci. 2014;34:16180–93.
pubmed: 25471560
pmcid: 4252540
doi: 10.1523/JNEUROSCI.3020-14.2014
Rasmussen MK, Mestre H, Nedergaard M. The glymphatic pathway in neurological disorders. Lancet Neurol. 2018;17:1016–24.
pubmed: 30353860
pmcid: 6261373
doi: 10.1016/S1474-4422(18)30318-1
Bolte AC, Lukens JR. Neuroimmune cleanup crews in brain injury. Trends Immunol. 2021;42:480–94.
pubmed: 33941486
pmcid: 8165004
doi: 10.1016/j.it.2021.04.003
Simon DW, McGeachy MJ, Bayır H, Clark RSB, Loane DJ, Kochanek PM. The far-reaching scope of neuroinflammation after traumatic brain injury. Nat Rev Neurol. 2017;13:572.
pubmed: 28776601
doi: 10.1038/nrneurol.2017.116
Braun M, Vaibhav K, Saad NM, Fatima S, Vender JR, Baban B, et al. White matter damage after traumatic brain injury: a role for damage associated molecular patterns. Biochim Biophys Acta Mol Basis Dis. 2017;1863:2614–26.
pubmed: 28533056
doi: 10.1016/j.bbadis.2017.05.020
Tehse J, Taghibiglou C. The overlooked aspect of excitotoxicity: glutamate-independent excitotoxicity in traumatic brain injuries. Eur J Neurosci. 2019;49:1157–70.
pubmed: 30554430
doi: 10.1111/ejn.14307
Khatri N, Thakur M, Pareek V, Kumar S, Sharma S, Datusalia AK. Oxidative stress: major threat in traumatic brain injury. CNS Neurol Disord Drug Targets. 2018;17:689–95.
pubmed: 29952272
doi: 10.2174/1871527317666180627120501
Stahel PF, Morganti-Kossmann MC, Perez D, Redaelli C, Gloor B, Trentz O, et al. Intrathecal levels of complement-derived soluble membrane attack complex (sC5b-9) correlate with blood-brain barrier dysfunction in patients with traumatic brain injury. J Neurotrauma. 2001;18:773–81.
pubmed: 11526983
doi: 10.1089/089771501316919139
Akeret K, Buzzi RM, Schaer CA, Thomson BR, Vallelian F, Wang S, et al. Cerebrospinal fluid hemoglobin drives subarachnoid hemorrhage-related secondary brain injury. J Cereb Blood Flow Metab. 2021;41:3000–15.
pubmed: 34102922
pmcid: 8545037
doi: 10.1177/0271678X211020629
Edwards G, Zhao J, Dash PK, Soto C, Moreno-Gonzalez I. Traumatic brain injury induces tau aggregation and spreading. J Neurotrauma. 2020;37:80–92.
pubmed: 31317824
doi: 10.1089/neu.2018.6348
Johnson VE, Stewart W, Smith DH. Traumatic brain injury and amyloid-β pathology: a link to Alzheimer’s disease? Nat Rev Neurosci. 2010;11:361–70.
pubmed: 20216546
pmcid: 3979339
doi: 10.1038/nrn2808
Polymenidou M, Cleveland DW. Prion-like spread of protein aggregates in neurodegeneration. J Exp Med. 2012;209:889–93.
pubmed: 22566400
pmcid: 3348110
doi: 10.1084/jem.20120741
Harris JA, Devidze N, Verret L, Ho K, Halabisky B, Thwin MT, et al. Transsynaptic progression of amyloid-β-induced neuronal dysfunction within the entorhinal-hippocampal network. Neuron. 2010;68:428–41.
pubmed: 21040845
pmcid: 3050043
doi: 10.1016/j.neuron.2010.10.020
Woerman AL, Aoyagi A, Patel S, Kazmi SA, Lobach I, Grinberg LT, et al. Tau prions from Alzheimer’s disease and chronic traumatic encephalopathy patients propagate in cultured cells. Proc Natl Acad Sci USA. 2016;113:E8187–96.
pubmed: 27911827
pmcid: 5167200
doi: 10.1073/pnas.1616344113
Hickman S, Izzy S, Sen P, Morsett L, el Khoury J. Microglia in neurodegeneration. Nat Neurosci. 2018;21:1359–69.
pubmed: 30258234
pmcid: 6817969
doi: 10.1038/s41593-018-0242-x
Deane R, Bell RD, Sagare A, Zlokovic BV. Clearance of amyloid-beta peptide across the blood-brain barrier: implication for therapies in Alzheimer’s disease. CNS Neurol Disord Drug Targets. 2009;8:16–30.
pubmed: 19275634
pmcid: 2872930
doi: 10.2174/187152709787601867
Pop V, Sorensen DW, Kamper JE, Ajao DO, Murphy MP, Head E, et al. Early brain injury alters the blood-brain barrier phenotype in parallel with β-amyloid and cognitive changes in adulthood. J Cereb Blood Flow Metab. 2013;33:205–14.
pubmed: 23149553
doi: 10.1038/jcbfm.2012.154
Bolte AC, Dutta AB, Hurt ME, Smirnov I, Kovacs MA, McKee CA, et al. Meningeal lymphatic dysfunction exacerbates traumatic brain injury pathogenesis. Nat Commun. 2020;11:4524.
pubmed: 32913280
pmcid: 7483525
doi: 10.1038/s41467-020-18113-4
Simon MJ, Iliff JJ. Regulation of cerebrospinal fluid (CSF) flow in neurodegenerative, neurovascular and neuroinflammatory disease. Biochim Biophys Acta. 2016;1862:442–51.
pubmed: 26499397
doi: 10.1016/j.bbadis.2015.10.014
Kaiser K, Bryja V. Choroid plexus: the orchestrator of long-range signalling within the CNS. Int J Mol Sci. 2020;21:4760.
pubmed: 32635478
pmcid: 7369786
doi: 10.3390/ijms21134760
Hladky SB, Barrand MA. Mechanisms of fluid movement into, through and out of the brain: evaluation of the evidence. Fluids Barriers CNS. 2014;11:26.
pubmed: 25678956
pmcid: 4326185
doi: 10.1186/2045-8118-11-26
Feinberg DA, Mark AS. Human brain motion and cerebrospinal fluid circulation demonstrated with MR velocity imaging. Radiology. 1987;163:793–9.
pubmed: 3575734
doi: 10.1148/radiology.163.3.3575734
Dreha-Kulaczewski S, Joseph AA, Merboldt K-D, Ludwig H-C, Gärtner J, Frahm J. Inspiration is the major regulator of human CSF flow. J Neurosci. 2015;35:2485–91.
pubmed: 25673843
pmcid: 6605608
doi: 10.1523/JNEUROSCI.3246-14.2015
Hansen EA, Romanova L, Janson C, Lam CH. The effects of blood and blood products on the arachnoid cell. Exp Brain Res. 2017;235:1749–58.
pubmed: 28285405
doi: 10.1007/s00221-017-4927-2
Dalkara T. Cerebral Microcirculation: an introduction | SpringerLink. 2022. https://link.springer.com/referenceworkentry/10.1007/978-3-642-37078-6_29 .
Tuma RF. The cerebral microcirculation. Microcirculation. 2nd Edition. 2008:485–520.
Bacyinski A, Xu M, Wang W, Hu J. The paravascular pathway for brain waste clearance: current understanding, significance and controversy. Front Neuroanat. 2017;11:101.
pubmed: 29163074
pmcid: 5681909
doi: 10.3389/fnana.2017.00101
Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JAR, Perry VH, et al. 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. 2008;34:131–44.
pubmed: 18208483
doi: 10.1111/j.1365-2990.2007.00926.x
Morris AWJ, Sharp MM, Albargothy NJ, Fernandes R, Hawkes CA, Verma A, et al. Vascular basement membranes as pathways for the passage of fluid into and out of the brain. Acta Neuropathol. 2016;131:725–36.
pubmed: 26975356
pmcid: 4835509
doi: 10.1007/s00401-016-1555-z
Faghih MM, Sharp MK. Is bulk flow plausible in perivascular, paravascular and paravenous channels? Fluids Barriers CNS. 2018;15:17.
pubmed: 29903035
pmcid: 6003203
doi: 10.1186/s12987-018-0103-8
Hershenhouse KS, Shauly O, Gould DJ, Patel KM. Meningeal lymphatics: a review and future directions from a clinical perspective. Neurosci Insights. 2019;14:1179069519889027.
pubmed: 32363346
pmcid: 7176397
doi: 10.1177/1179069519889027
Aspelund A, Antila S, Proulx ST, Karlsen TV, Karaman S, Detmar M, et al. A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med. 2015;212:991–9.
pubmed: 26077718
pmcid: 4493418
doi: 10.1084/jem.20142290
Yankova G, Bogomyakova O, Tulupov A. The glymphatic system and meningeal lymphatics of the brain: new understanding of brain clearance. Rev Neurosci. 2021;32:693–705.
pubmed: 33618444
doi: 10.1515/revneuro-2020-0106
Nedergaard M. Neuroscience. Garbage truck of the brain. Science. 2013;340:1529–30.
pubmed: 23812703
pmcid: 3749839
doi: 10.1126/science.1240514
Engelhardt B, Coisne C. Fluids and barriers of the CNS establish immune privilege by confining immune surveillance to a two-walled castle moat surrounding the CNS castle. Fluids Barriers CNS. 2011;8:4.
pubmed: 21349152
pmcid: 3039833
doi: 10.1186/2045-8118-8-4
Mathiisen TM, Lehre KP, Danbolt NC, Ottersen OP. The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction. Glia. 2010;58:1094–103.
pubmed: 20468051
doi: 10.1002/glia.20990
Simard M, Arcuino G, Takano T, Liu QS, Nedergaard M. Signaling at the gliovascular interface. J Neurosci. 2003;23:9254–62.
pubmed: 14534260
pmcid: 6740832
doi: 10.1523/JNEUROSCI.23-27-09254.2003
Jessen NA, Munk ASF, Lundgaard I, Nedergaard M. The glymphatic system: a beginner’s guide. Neurochem Res. 2015;40:2583–99.
pubmed: 25947369
pmcid: 4636982
doi: 10.1007/s11064-015-1581-6
Salman MM, Kitchen P, Halsey A, Wang MX, Törnroth-Horsefield S, Conner AC, et al. Emerging roles for dynamic aquaporin-4 subcellular relocalization in CNS water homeostasis. Brain. 2022;145:64–75.
pubmed: 34499128
doi: 10.1093/brain/awab311
Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci. 1997;17:171–80.
pubmed: 8987746
pmcid: 6793699
doi: 10.1523/JNEUROSCI.17-01-00171.1997
Neely JD, Amiry-Moghaddam M, Ottersen OP, Froehner SC, Agre P, Adams ME. Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein. Proc Natl Acad Sci USA. 2001;98:14108–13.
pubmed: 11717465
pmcid: 61176
doi: 10.1073/pnas.241508198
Amiry-Moghaddam M, Frydenlund DS, Ottersen OP. Anchoring of aquaporin-4 in brain: molecular mechanisms and implications for the physiology and pathophysiology of water transport. Neuroscience. 2004;129:999–1010.
pubmed: 15561415
doi: 10.1016/j.neuroscience.2004.08.049
Szczygielski J, Kopańska M, Wysocka A, Oertel J. Cerebral microcirculation, perivascular unit, and glymphatic system: role of aquaporin-4 as the gatekeeper for water homeostasis. Front Neurol. 2021;12:767470.
pubmed: 34966347
pmcid: 8710539
doi: 10.3389/fneur.2021.767470
Johnston M, Zakharov A, Papaiconomou C, Salmasi G, Armstrong D. Evidence of connections between cerebrospinal fluid and nasal lymphatic vessels in humans, non-human primates and other mammalian species. Cerebrospinal Fluid Res. 2004;1:2.
pubmed: 15679948
pmcid: 546409
doi: 10.1186/1743-8454-1-2
Moshkforoush A, Ashenagar B, Harraz OF, Dabertrand F, Longden TA, Nelson MT, et al. The capillary Kir channel as sensor and amplifier of neuronal signals: modeling insights on K+-mediated neurovascular communication. Proc Natl Acad Sci USA. 2020;117:16626–37.
pubmed: 32601236
pmcid: 7368319
doi: 10.1073/pnas.2000151117
MacAulay N. Molecular mechanisms of K+ clearance and extracellular space shrinkage-glia cells as the stars. Glia. 2020;68:2192–211.
pubmed: 32181522
doi: 10.1002/glia.23824
Iadecola C. The neurovascular unit coming of age: a journey through neurovascular coupling in health and disease. Neuron. 2017;96:17–42.
pubmed: 28957666
pmcid: 5657612
doi: 10.1016/j.neuron.2017.07.030
Schaeffer S, Iadecola C. Revisiting the neurovascular unit. Nat Neurosci. 2021;24:1198–209.
pubmed: 34354283
pmcid: 9462551
doi: 10.1038/s41593-021-00904-7
Benveniste H, Heerdt PM, Fontes M, Rothman DL, Volkow ND. Glymphatic system function in relation to anesthesia and sleep states. Anesth Analg. 2019;128:747–58.
pubmed: 30883420
doi: 10.1213/ANE.0000000000004069
Fultz NE, Bonmassar G, Setsompop K, Stickgold RA, Rosen BR, Polimeni JR, et al. Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep. Science. 2019;366:628–31.
pubmed: 31672896
pmcid: 7309589
doi: 10.1126/science.aax5440
Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, et al. Sleep drives metabolite clearance from the adult brain. Science. 2013;342:373–7.
pubmed: 24136970
doi: 10.1126/science.1241224
Reddy OC, van der Werf YD. The sleeping brain: harnessing the power of the glymphatic system through lifestyle choices. Brain Sci. 2020;10:868.
pubmed: 33212927
pmcid: 7698404
doi: 10.3390/brainsci10110868
Myung J, Wu D, Simonneaux V, Lane TJ. Strong circadian rhythms in the choroid plexus: implications for sleep-independent brain metabolite clearance. J Exp Neurosci. 2018;12:1179069518783762.
pubmed: 30013386
pmcid: 6043913
doi: 10.1177/1179069518783762
Christensen J, Li C, Mychasiuk R. Choroid plexus function in neurological homeostasis and disorders: the awakening of the circadian clocks and orexins. J Cereb Blood Flow Metab. 2022;42:1163–75.
pubmed: 35296175
pmcid: 9207490
doi: 10.1177/0271678X221082786
Li L, Chopp M, Ding G, Davoodi-Bojd E, Zhang L, Li Q, et al. MRI detection of impairment of glymphatic function in rat after mild traumatic brain injury. Brain Res. 2020;1747:147062.
pubmed: 32818526
pmcid: 9419050
doi: 10.1016/j.brainres.2020.147062
Christensen J, Wright DK, Yamakawa GR, Shultz SR, Mychasiuk R. Repetitive mild traumatic brain injury alters glymphatic clearance rates in limbic structures of adolescent female rats. Sci Rep. 2020;10:6254.
pubmed: 32277097
pmcid: 7148360
doi: 10.1038/s41598-020-63022-7
Gama Sosa MA, de Gasperi R, Pryor D, Perez Garcia GS, Perez GM, Abutarboush R, et al. Low-level blast exposure induces chronic vascular remodeling, perivascular astrocytic degeneration and vascular-associated neuroinflammation. Acta Neuropathol Commun. 2021;9:167.
pubmed: 34654480
pmcid: 8518227
doi: 10.1186/s40478-021-01269-5
Ren Z, Iliff JJ, Yang L, Yang J, Chen X, Chen MJ, et al. ‘Hit & Run’ model of closed-skull traumatic brain injury (TBI) reveals complex patterns of post-traumatic AQP4 dysregulation. J Cereb Blood Flow Metab. 2013;33:834–45.
pubmed: 23443171
pmcid: 3677112
doi: 10.1038/jcbfm.2013.30
Liu X, Xie Y, Wan X, Wu J, Fan Z, Yang L. Protective effects of aquaporin-4 deficiency on longer-term neurological outcomes in a mouse model. Neurochem Res. 2021;46:1380–9.
pubmed: 33651262
doi: 10.1007/s11064-021-03272-7
Katada R, Akdemir G, Asavapanumas N, Ratelade J, Zhang H, Verkman AS. Greatly improved survival and neuroprotection in aquaporin-4-knockout mice following global cerebral ischemia. FASEB J. 2014;28:705–14.
pubmed: 24186965
pmcid: 3898642
doi: 10.1096/fj.13-231274
Ramirez J, Berezuk C, McNeely AA, Gao F, McLaurin J, Black SE. Imaging the perivascular space as a potential biomarker of neurovascular and neurodegenerative diseases. Cell Mol Neurobiol. 2016;36:289–99.
pubmed: 26993511
doi: 10.1007/s10571-016-0343-6
Doubal FN, MacLullich AMJ, Ferguson KJ, Dennis MS, Wardlaw JM. Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke. 2010;41:450–4.
pubmed: 20056930
doi: 10.1161/STROKEAHA.109.564914
Bokura H, Kobayashi S, Yamaguchi S. Distinguishing silent lacunar infarction from enlarged Virchow-Robin spaces: a magnetic resonance imaging and pathological study. J Neurol. 1998;245:116–22.
pubmed: 9507419
doi: 10.1007/s004150050189
Adams HHH, Cavalieri M, Verhaaren BFJ, Bos D, van der Lugt A, Enzinger C, et al. Rating method for dilated Virchow-Robin spaces on magnetic resonance imaging. Stroke. 2013;44:1732–5.
pubmed: 23640831
doi: 10.1161/STROKEAHA.111.000620
Hilal S, Tan CS, Adams HHH, Habes M, Mok V, Venketasubramanian N, et al. Enlarged perivascular spaces and cognition: a meta-analysis of 5 population-based studies. Neurology. 2018;91:e832–42.
pubmed: 30068634
pmcid: 6133622
doi: 10.1212/WNL.0000000000006079
Vilor-Tejedor N, Ciampa I, Operto G, Falcón C, Suárez-Calvet M, Crous-Bou M, et al. Perivascular spaces are associated with tau pathophysiology and synaptic dysfunction in early Alzheimer’s continuum. Alzheimers Res Ther. 2021;13:135.
pubmed: 34353353
pmcid: 8340485
doi: 10.1186/s13195-021-00878-5
Tu Y, Zhuo W, Peng J, Huang R, Li B, Liu Y, et al. The correlation between enlarged perivascular spaces and cognitive impairment in Parkinson’s disease and vascular parkinsonism. BMC Neurol. 2022;22:282.
pubmed: 35906550
pmcid: 9336003
doi: 10.1186/s12883-022-02819-7
Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, et al. Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest. 2013;123:1299–309.
pubmed: 23434588
pmcid: 3582150
doi: 10.1172/JCI67677
Ringstad G, Vatnehol SAS, Eide PK. Glymphatic MRI in idiopathic normal pressure hydrocephalus. Brain. 2017;140:2691–705.
pubmed: 28969373
pmcid: 5841149
doi: 10.1093/brain/awx191
Ahn SJ, Taoka T, Moon W-J, Naganawa S. Contrast-enhanced fluid-attenuated inversion recovery in neuroimaging: a narrative review on clinical applications and technical advances. J Magn Reson Imaging. 2022;56:341–53.
pubmed: 35170148
doi: 10.1002/jmri.28117
Wong SM, Backes WH, Drenthen GS, Zhang CE, Voorter PHM, Staals J, et al. Spectral diffusion analysis of intravoxel incoherent motion MRI in cerebral small vessel disease. J Magn Reson Imaging. 2020;51:1170–80.
pubmed: 31486211
doi: 10.1002/jmri.26920
Huang J, van Zijl PCM, Han X, Dong CM, Cheng GWY, Tse K-H, et al. Altered d-glucose in brain parenchyma and cerebrospinal fluid of early Alzheimer’s disease detected by dynamic glucose-enhanced MRI. Sci Adv. 2020;6:eaba3884.
pubmed: 32426510
pmcid: 7220384
doi: 10.1126/sciadv.aba3884
Kiviniemi V, Wang X, Korhonen V, Keinänen T, Tuovinen T, Autio J, et al. Ultra-fast magnetic resonance encephalography of physiological brain activity—glymphatic pulsation mechanisms? J Cereb Blood Flow Metab. 2016;36:1033–45.
pubmed: 26690495
doi: 10.1177/0271678X15622047
Newell DW, Nedergaard M, Aaslid R. Physiological mechanisms and significance of intracranial B waves. Front Neurol. 2022;13:872701.
pubmed: 35651339
pmcid: 9149212
doi: 10.3389/fneur.2022.872701
Piantino JA, Iliff JJ, Lim MM. The bidirectional link between sleep disturbances and traumatic brain injury symptoms: a role for glymphatic dysfunction? Biol Psychiatry. 2022;91:478–87.
pubmed: 34481662
doi: 10.1016/j.biopsych.2021.06.025
Christensen J, Yamakawa GR, Shultz SR, Mychasiuk R. Is the glymphatic system the missing link between sleep impairments and neurological disorders? Examining the implications and uncertainties. Prog Neurobiol. 2021;198:101917.
pubmed: 32991958
doi: 10.1016/j.pneurobio.2020.101917
Mathias JL, Alvaro PK. Prevalence of sleep disturbances, disorders, and problems following traumatic brain injury: a meta-analysis. Sleep Med. 2012;13:898–905.
pubmed: 22705246
doi: 10.1016/j.sleep.2012.04.006
Parcell DL, Ponsford JL, Redman JR, Rajaratnam SM. Poor sleep quality and changes in objectively recorded sleep after traumatic brain injury: a preliminary study. Arch Phys Med Rehabil. 2008;89:843–50.
pubmed: 18452730
doi: 10.1016/j.apmr.2007.09.057
Chaput G, Giguère J-F, Chauny J-M, Denis R, Lavigne G. Relationship among subjective sleep complaints, headaches, and mood alterations following a mild traumatic brain injury. Sleep Med. 2009;10:713–6.
pubmed: 19147402
doi: 10.1016/j.sleep.2008.07.015
Wickwire EM, Williams SG, Roth T, Capaldi VF, Jaffe M, Moline M, et al. Sleep, sleep disorders, and mild traumatic brain injury. What we know and what we need to know: findings from a National Working Group. Neurotherapeutics. 2016;13:403–17.
pubmed: 27002812
pmcid: 4824019
doi: 10.1007/s13311-016-0429-3
Piantino J, Lim MM, Newgard CD, Iliff J. Linking traumatic brain injury, sleep disruption and post-traumatic headache: a potential role for glymphatic pathway dysfunction. Curr Pain Headache Rep. 2019;23:62.
pubmed: 31359173
doi: 10.1007/s11916-019-0799-4
Sandsmark DK, Elliott JE, Lim MM. Sleep-wake disturbances after traumatic brain injury: synthesis of human and animal studies. Sleep. 2017;40:zsx044.
pubmed: 28329120
pmcid: 6251652
Opel RA, Christy A, Boespflug EL, Weymann KB, Case B, Pollock JM, et al. Effects of traumatic brain injury on sleep and enlarged perivascular spaces. J Cereb Blood Flow Metab. 2019;39:2258–67.
pubmed: 30092696
doi: 10.1177/0271678X18791632
Piantino J, Schwartz DL, Luther M, Newgard C, Silbert L, Raskind M, et al. Link between mild traumatic brain injury, poor sleep, and magnetic resonance imaging: visible perivascular spaces in veterans. J Neurotrauma. 2021;38:2391–9.
pubmed: 33599176
pmcid: 8390772
doi: 10.1089/neu.2020.7447
Mondello S, Muller U, Jeromin A, Streeter J, Hayes RL, Wang KKW. Blood-based diagnostics of traumatic brain injuries. Expert Rev Mol Diagn. 2011;11:65–78.
pubmed: 21171922
pmcid: 3063529
doi: 10.1586/erm.10.104
Chodobski A, Zink BJ, Szmydynger-Chodobska J. Blood-brain barrier pathophysiology in traumatic brain injury. Transl Stroke Res. 2011;2:492–516.
pubmed: 22299022
pmcid: 3268209
doi: 10.1007/s12975-011-0125-x
McDonald SJ, Shultz SR, Agoston DV. The known unknowns: an overview of the state of blood-based protein biomarkers of mild traumatic brain injury. J Neurotrauma. 2021;38:2652–66.
pubmed: 33906422
doi: 10.1089/neu.2021.0011
Plog BA, Dashnaw ML, Hitomi E, Peng W, Liao Y, Lou N, et al. Biomarkers of traumatic injury are transported from brain to blood via the glymphatic system. J Neurosci. 2015;35:518–26.
pubmed: 25589747
pmcid: 4293408
doi: 10.1523/JNEUROSCI.3742-14.2015
Plog BA, Nedergaard M. Why have we not yet developed a simple blood test for TBI? Expert Rev Neurother. 2015;15:465–8.
pubmed: 25821902
doi: 10.1586/14737175.2015.1031112
Lindblad C, Nelson DW, Zeiler FA, Ercole A, Ghatan PH, von Horn H, et al. Influence of blood-brain barrier integrity on brain protein biomarker clearance in severe traumatic brain injury: a longitudinal prospective study. J Neurotrauma. 2020;37:1381–91.
pubmed: 32013731
pmcid: 7249468
doi: 10.1089/neu.2019.6741
Murcko R, Marchi N, Bailey D, Janigro D. Diagnostic biomarker kinetics: how brain-derived biomarkers distribute through the human body, and how this affects their diagnostic significance: the case of S100B. Fluids Barriers CNS. 2022;19:32.
pubmed: 35546671
pmcid: 9092835
doi: 10.1186/s12987-022-00329-9
Xuan X, Zhou G, Chen C, Shao A, Zhou Y, Li X, et al. Glymphatic system: emerging therapeutic target for neurological diseases. Oxid Med Cell Longev. 2022;2022:6189170.
pubmed: 35726332
pmcid: 9206554
doi: 10.1155/2022/6189170
Sun B-L, Wang L-H, Yang T, Sun J-Y, Mao L-L, Yang M-F, et al. Lymphatic drainage system of the brain: a novel target for intervention of neurological diseases. Prog Neurobiol. 2018;163-4:118–43.
doi: 10.1016/j.pneurobio.2017.08.007
Cherian I, Bernardo A, Grasso G. Cisternostomy for traumatic brain injury: pathophysiologic mechanisms and surgical technical notes. World Neurosurg. 2016;89:51–7.
pubmed: 26851743
doi: 10.1016/j.wneu.2016.01.072
Cherian I, Burhan H, Dashevskiy G, Motta SJH, Parthiban J, Wang Y, et al. Cisternostomy: a timely intervention in moderate to severe traumatic brain injuries: rationale, indications, and prospects. World Neurosurg. 2019;131:385–90.
pubmed: 31658580
doi: 10.1016/j.wneu.2019.07.082
Goyal N, Kumar P. Putting ‘CSF-Shift Edema’ hypothesis to test: comparing cisternal and parenchymal pressures after basal cisternostomy for head injury. World Neurosurg. 2021;148:e252–63.
pubmed: 33412318
doi: 10.1016/j.wneu.2020.12.133
Zhou Y, Shao A, Xu W, Wu H, Deng Y. Advance of stem cell treatment for traumatic brain injury. Front Cell Neurosci. 2019;13:301.
pubmed: 31456663
pmcid: 6700304
doi: 10.3389/fncel.2019.00301
Zhang E, Wan X, Yang L, Wang D, Chen Z, Chen Y, et al. Omega-3 polyunsaturated fatty acids alleviate traumatic brain injury by regulating the glymphatic pathway in mice. Front Neurol. 2020;11:707.
pubmed: 32765412
pmcid: 7380115
doi: 10.3389/fneur.2020.00707
Kannan G, Kambhampati SP, Kudchadkar SR. Effect of anesthetics on microglial activation and nanoparticle uptake: implications for drug delivery in traumatic brain injury. J Control Release. 2017;263:192–9.
pubmed: 28336376
doi: 10.1016/j.jconrel.2017.03.032
Sachdeva S, Persaud S, Patel M, Popard P, Colverson A, Doré S. Effects of sound interventions on the permeability of the blood-brain barrier and meningeal lymphatic clearance. Brain Sci. 2022;12:742.
pubmed: 35741627
pmcid: 9221168
doi: 10.3390/brainsci12060742
Guernsey DT, Leder A, Yao S. Resolution of concussion symptoms after osteopathic manipulative treatment: a case report. J Am Osteopath Assoc. 2016;116:e13–7.
pubmed: 26927914
Kratz SV. Case report: Manual therapies promote resolution of persistent post-concussion symptoms in a 24-year-old athlete. SAGE Open Med Case Rep. 2021;9:2050313X20952224.
pubmed: 33628444
pmcid: 7829464
Kashyap S, Brazdzionis J, Savla P, Berry JA, Farr S, Patchana T, et al. Osteopathic manipulative treatment to optimize the glymphatic environment in severe traumatic brain injury measured with optic nerve sheath diameter, intracranial pressure monitoring, and neurological pupil index. Cureus. 2021;13:e13823.
pubmed: 33859888
pmcid: 8038899
Kress BT, Iliff JJ, Xia M, Wang M, Wei HS, Zeppenfeld D, et al. Impairment of paravascular clearance pathways in the aging brain. Ann Neurol. 2014;76:845–61.
pubmed: 25204284
pmcid: 4245362
doi: 10.1002/ana.24271
Xu Z, Xiao N, Chen Y, Huang H, Marshall C, Gao J, et al. Deletion of aquaporin-4 in APP/PS1 mice exacerbates brain Aβ accumulation and memory deficits. Mol Neurodegener. 2015;10:58.
pubmed: 26526066
pmcid: 4631089
doi: 10.1186/s13024-015-0056-1
Zeppenfeld DM, Simon M, Haswell JD, D’Abreo D, Murchison C, Quinn JF, et al. Association of perivascular localization of aquaporin-4 with cognition and Alzheimer disease in aging brains. JAMA Neurol. 2017;74:91–9.
pubmed: 27893874
doi: 10.1001/jamaneurol.2016.4370
Zou W, Pu T, Feng W, Lu M, Zheng Y, Du R, et al. Blocking meningeal lymphatic drainage aggravates Parkinson’s disease-like pathology in mice overexpressing mutated α-synuclein. Transl Neurodegener. 2019;8:7.
pubmed: 30867902
pmcid: 6396507
doi: 10.1186/s40035-019-0147-y
Kanaan NM, Cox K, Alvarez VE, Stein TD, Poncil S, McKee AC. Characterization of early pathological tau conformations and phosphorylation in chronic traumatic encephalopathy. J Neuropathol Exp Neurol. 2016;75:19–34.
pubmed: 26671985
doi: 10.1093/jnen/nlv001