Glymphatic MRI in idiopathic normal pressure hydrocephalus

Brain

Volumn 140, Issue 10, 2017, Pages 2691-2705

  Ringstad, Geir ^a,b   Vatnehol, Svein Are Sirirud ^a   Eide, Per Kristian ^a,b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

cerebrospinal fluid; gadobutrol; glymphatic function; idiopathic normal pressure hydrocephalus; MRI

Indexed keywords

GADOBUTROL; IODIXANOL; CONTRAST MEDIUM; ORGANOMETALLIC COMPOUND;

AGED; ARTICLE; BRAIN CORTEX; BRAIN CYST; BRAIN FOURTH VENTRICLE; BRAIN METABOLISM; BRAIN THIRD VENTRICLE; BRAIN TISSUE; CEREBROSPINAL FLUID FLOW; CLINICAL ARTICLE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; EXTRAVASCULAR SPACE; FEMALE; FORAMEN MAGNUM; GLIA; GLYMPHATIC SYSTEM; HUMAN; IMAGE ANALYSIS; INFERIOR FRONTAL GYRUS; INTRACRANIAL HYPOTENSION; INTRACRANIAL PRESSURE MONITORING; LATERAL BRAIN VENTRICLE; LEPTOMENINX; LIQUORRHEA; LYMPHATIC SYSTEM; MALE; NORMOTENSIVE HYDROCEPHALUS; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; OBSERVATIONAL STUDY; PONS; PRECENTRAL SULCUS; PREPONTINE CISTERN; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PROSPECTIVE STUDY; SLEEP; SUBARACHNOID SPACE; SUPERIOR SAGITTAL SINUS; SUPINE POSITION; SYLVIAN FISSURE; THALAMUS; ADULT; CEREBROSPINAL FLUID; DIAGNOSTIC IMAGING; IMAGE PROCESSING; MIDDLE AGED; PATHOLOGY; PROCEDURES; TIME FACTOR; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; CONTRAST MEDIA; FEMALE; HUMANS; HYDROCEPHALUS, NORMAL PRESSURE; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; ORGANOMETALLIC COMPOUNDS; PROSPECTIVE STUDIES; SUBARACHNOID SPACE; TIME FACTORS;

EID: 85030707725     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awx191     Document Type: Article

References (51)

1. Adams RD, Fisher CM, Hakim S, Ojemann RG, Sweet WH. Symptomatic occult hydrocephalus with "Normal" cerebrospinalfluid pressure. A treatable syndrome. N Eng J Med 1965; 273: 117-26.
2. Akbar JJ, Luetmer PH, Schwartz KM, Hunt CH, Diehn FE, Eckel LJ. The role of MR myelography with intrathecal gadolinium in localization of spinal CSF leaks in patients with spontaneous intracranial hypotension. AJNR Am J Neuroradiol 2012; 33: 535-40.
3. Asgari M, de Zelicourt D, Kurtcuoglu V. Glymphatic solute transport does not require bulk flow. Sci Rep 2016; 6: 38635.
4. Aydin K, Guven K, Sencer S, Jinkins JR, Minareci O. MRI cisternography with gadolinium-containing contrast medium: its role, advantages and limitations in the investigation of rhinorrhoea. Neuroradiology 2004; 46: 75-80.
5. Bakker EN, Bacskai BJ, Arbel-Ornath M, Aldea R, Bedussi B, Morris AW, et al. Lymphatic clearance of the brain: perivascular, paravascular and significance for neurodegenerative diseases. Cell Mol Neurobiol 2016; 36: 181-94.
6. Bedussi B, van der Wel NN, de Vos J, van Veen H, Siebes M, VanBavel E, et al. Paravascular channels, cisterns, and the subarachnoid space in the rat brain: A single compartment with preferential pathways. J Cereb Blood Flow Metab 2017; 37: 1374-85.
7. Bering EA Jr, Sato O. Hydrocephalus: changes in formation and absorption of cerebrospinal fluid within the cerebral ventricles. J Neurosurg 1963; 20: 1050-63.
8. Bradley WG Jr, Scalzo D, Queralt J, Nitz WN, Atkinson DJ, Wong P. Normal-pressure hydrocephalus: evaluation with cerebrospinal fluid flow measurements at MR imaging. Radiology 1996; 198: 523-9.
9. Cabral D, Beach TG, Vedders L, Sue LI, Jacobson S, Myers K, et al. Frequency of Alzheimer's disease pathology at autopsy in patients with clinical normal pressure hydrocephalus. Alzheimers Dement 2011; 7: 509-13.
10. Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JA, 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.
11. Cheng KT. Gadobutrol. Molecular Imaging and Contrast Agent Database (MICAD). Bethesda, MD: National Center for Biotechnology Information (US); 2004.
12. Eide PK. Demonstration of uneven distribution of intracranial pulsatility in hydrocephalus patients. J Neurosurg 2008; 109: 912-17.
13. Eide PK, Eidsvaag VA, Nagelhus EA, Hansson HA. Cortical astrogliosis and increased perivascular aquaporin-4 in idiopathic intracranial hypertension. Brain Res 2016; 1644: 161-75.
14. Eide PK, Ringstad G. MRI with intrathecal MRI gadolinium contrast medium administration: A possible method to assess glymphatic function in human brain. Acta Radiol Open 2015; 4: 2058460115609635.
15. Eide PK, Saehle T. Is ventriculomegaly in idiopathic normal pressure hydrocephalus associated with a transmantle gradient in pulsatile intracranial pressure Acta Neurochir 2010; 152: 989-95.
16. Eide PK, Sorteberg W. Diagnostic intracranial pressure monitoring and surgical management in idiopathic normal pressure hydrocephalus: A 6-year review of 214 patients. Neurosurgery 2010; 66: 80-91.
17. Gideon P, Thomsen C, Gjerris F, Sorensen PS, Henriksen O. Increased self-diffusion of brain water in hydrocephalus measured by MR imaging. Acta Radiol 1994; 35: 514-19.
18. Greitz D. Radiological assessment of hydrocephalus: new theories and implications for therapy. Neurosurg Rev 2004; 27: 145-65; discussion 166-7.
19. Hashimoto M, Ishikawa M, Mori E, Kuwana N. Diagnosis of idiopathic normal pressure hydrocephalus is supported by MRI-based scheme: A prospective cohort study. Cerebrospinal Fluid Res 2010; 7: 18.
20. Heinz ER, Davis DO, Karp HR. Abnormal isotope cisternography in sympatomatic occult hydrocephalus. A correlative isotopic-neuroradiological study in 130 subjects. Radiology 1970; 95: 109-20.
21. 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.
22. Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, et al. Brainwide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest 2013a; 123: 1299-309.
23. 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 beta. Sci Transl Med 2012; 4: 147ra111.
24. Iliff JJ, Wang M, Zeppenfeld DM, Venkataraman A, Plog BA, Liao Y, et al. Cerebral arterial pulsation drives paravascular CSF-interstitial fluid exchange in the murine brain. J Neurosci 2013b; 33: 18190-9.
25. Ishikawa M, Yamada S, Yamamoto K. Three-dimensional observation of Virchow-Robin spaces in the basal ganglia and white matter and their relevance to idiopathic normal pressure hydrocephalus. Fluids Barriers CNS 2015; 12: 15.
26. Iwamoto T, Miyaji H, Kanaya K, Takasaki M. Periventricular lucency evaluated by second-derivative finger plethysmography. Geriatr Gerontol Int 2001; 1: 25-32.
27. Jessen NA, Munk AS, Lundgaard I, Nedergaard M. The glymphatic system: A beginner's guide. Neurochem Res 2015; 40: 2583-99.
28. Jin BJ, Smith AJ, Verkman AS. Spatial model of convective solute transport in brain extracellular space does not support a "glymphatic" mechanism. J Gen Physiol 2016; 148: 489-501.
29. Jinkins JR, Rudwan M, Krumina G, Tali ET. Intrathecal gadoliniumenhanced MR cisternography in the evaluation of clinically suspected cerebrospinal fluid rhinorrhea in humans: early experience. Radiology 2002; 222: 555-9.
30. Kojoukhova M, Vanha KI, Timonen M, Koivisto AM, Nerg O, Rummukainen J, et al. Associations of intracranial pressure with brain biopsy, radiological findings, and shunt surgery outcome in patients with suspected idiopathic normal pressure hydrocephalus. Acta Neurochir 2017; 159: 51-61.
31. 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.
32. Lee H, Xie L, Yu M, Kang H, Feng T, Deane R, et al. The effect of body posture on brain glymphatic transport. J Neurosci 2015; 35: 11034-44.
33. Levine DN. Intracranial pressure and ventricular expansion in hydrocephalus: have we been asking the wrong question J Neurol Sci 2008; 269: 1-11.
34. Linninger AA, Tsakiris C, Zhu DC, Xenos M, Roycewicz P, Danziger Z, et al. Pulsatile cerebrospinal fluid dynamics in the human brain. IEEE Trans Biomed Eng 2005; 52: 557-65.
35. Lohrke J, Frenzel T, Endrikat J, Alves FC, Grist TM, Law M, et al. 25 years of contrast-enhanced MRI: developments, current challenges and future perspectives. Adv Ther 2016; 33: 1-28.
36. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, et al. Structural and functional features of central nervous system lymphatic vessels. Nature 2015; 523: 337-41.
37. Malayeri AA, Brooks KM, Bryant LH, Evers R, Kumar P, Reich DS, et al. National Institutes of Health perspective on reports of gadolinium deposition in the brain. J Am Coll Radiol 2016; 13: 237-41.
38. Nagelhus EA, Ottersen OP. Physiological roles of aquaporin-4 in brain. Physiol Rev 2013; 93: 1543-62.
39. Penn RD, Basati S, Sweetman B, Guo X, Linninger A. Ventricle wall movements and cerebrospinal fluid flow in hydrocephalus. J Neurosurg 2011; 115: 159-64.
40. 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.
41. Reiche W, Komenda Y, Schick B, Grunwald I, Steudel WI, Reith W. MR cisternography after intrathecal Gd-DTPA application. Eur Radiol 2002; 12: 2943-9.
42. Ringstad G, Emblem KE, Eide PK. Phase-contrast magnetic resonance imaging reveals net retrograde aqueductal flow in idiopathic normal pressure hydrocephalus. J Neurosurg 2016; 124: 1850-7.
43. Sahar A, Hochwald GM, Ransohoff J. Alternate pathway for cerebrospinal fluid absorption in animals with experimental obstructive hydrocephalus. Exp Neurol 1969; 25: 200-6.
44. Tarasoff-Conway JM, Carare RO, Osorio RS, Glodzik L, Butler T, Fieremans E, et al. Clearance systems in the brain-implications for Alzheimer diseaser. Nat Rev Neurol 2016; 12: 248.
45. van Swieten JC, Hijdra A, Koudstaal PJ, van Gijn J. Grading white matter lesions on CT and MRI: A simple scale. J Neurol Neurosurg Psychiatry 1990; 53: 1080-3.
46. Vindedal GF, Thoren AE, Jensen V, Klungland A, Zhang Y, Holtzman MJ, et al. Removal of aquaporin-4 from glial and ependymal membranes causes brain water accumulation. Mol Cell Neurosci 2016; 77: 47-52.
47. Weller RO. Microscopic morphology and histology of the human meninges. Morphologie 2005; 89: 22-34.
48. Weller RO, Boche D, Nicoll JA. Microvasculature changes and cerebral amyloid angiopathy in Alzheimer's disease and their potential impact on therapy. Acta Neuropathol 2009; 118: 87-102.
49. 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.
50. Yang L, Kress BT, Weber HJ, Thiyagarajan M, Wang B, Deane R, et al. Evaluating glymphatic pathway function utilizing clinically relevant intrathecal infusion of CSF tracer. J Transl Med 2013; 11: 107.
51. Yin LK, Zheng JJ, Zhao L, Hao XZ, Zhang XX, Tian JQ, et al. Reversed aqueductal cerebrospinal fluid net flow in idiopathic normal pressure hydrocephalus. Acta Neurol Scand 2017. [Epub ahead of print]. doi: 10.1111/ane.12750.