Cerebrospinal fluid is drained primarily via the spinal canal and olfactory route in young and aged spontaneously hypertensive rats

Fluids and Barriers of the CNS

Volumn 11, Issue 1, 2014, Pages

  Murtha, Lucy A ^a   Yang, Qing ^b   Parsons, Mark W ^c   Levi, Christopher R ^c   Beard, Daniel J ^a   Spratt, Neil J ^a,c   McLeod, Damian D ^a  

^a HUNTER MEDICAL RESEARCH INSTITUTE   (Australia)

^b Apollo Medical Imaging Technology Pty Ltd   (Australia)

^c JOHN HUNTER HOSPITAL   (Australia)

Author keywords

Age; Cerebrospinal fluid dynamics; Computed tomography; Contrast; CSF; Intracranial pressure (ICP); SHR; Spontaneously hypertensive rat

Indexed keywords

AGED; ANIMAL EXPERIMENT; ARTICLE; BRAIN AQUEDUCT; BRAIN SIZE; CEREBROSPINAL FLUID DRAINAGE; CEREBROSPINAL FLUID FLOW; COMPUTED TOMOGRAPHY SCANNER; COMPUTER ASSISTED TOMOGRAPHY; COMPUTER PROGRAM; CONTRAST ENHANCEMENT; CONTROLLED STUDY; FLOW RATE; IN VIVO STUDY; INTRACRANIAL PRESSURE; LATERAL BRAIN VENTRICLE; MALE; NERVOUS SYSTEM PARAMETERS; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY SYSTEM; PRIORITY JOURNAL; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; SUPERIOR SAGITTAL SINUS; VERTEBRAL CANAL;

EID: 84902544568     PISSN: None     EISSN: 20458118     Source Type: Journal    
DOI: 10.1186/2045-8118-11-12     Document Type: Article

References (61)

1. Wagshul ME, McAllister JP, Rashid S, Li J, Egnor MR, Walker ML, Yu M, Smith SD, Zhang G, Chen JJ, Benveniste H. Ventricular dilation and elevated aqueductal pulsations in a new experimental model of communicating hydrocephalus. Exp Neurol 2009, 218:33-40. 10.1016/j.expneurol.2009.03.034, 19348801.
2. Bateman GA. The pathophysiology of idiopathic normal pressure hydrocephalus: cerebral ischemia or altered venous hemodynamics?. AJNR Am J Neuroradiol 2008, 29:198-203. 10.3174/ajnr.A0739, 17925373.
3. Preuss M, Hoffmann KT, Reiss-Zimmermann M, Hirsch W, Merkenschlager A, Meixensberger J, Dengl M. Updated physiology and pathophysiology of CSF circulation-the pulsatile vector theory. Childs Nerv Syst 2013, 29:1811-1825. 10.1007/s00381-013-2219-0, 23832074.
4. Killer HE, Jaggi GP, Flammer J, Miller NR, Huber AR, Mironov A. Cerebrospinal fluid dynamics between the intracranial and the subarachnoid space of the optic nerve. Is it always bidirectional?. Brain 2007, 130:514-520. 10.1093/brain/awl324, 17114796.
5. Shapira Y, Artru AA, Lam AM. Changes in the rate of formation and resistance to reabsorption of cerebrospinal fluid during deliberate hypotension induced with adenosine or hemorrhage. Anesthesiology 1992, 76:432-439. 10.1097/00000542-199203000-00017, 1539856.
6. Paradot G, Baledent O, Gondry-Jouet C, Meyer ME, Le Gars D. [Cerebrospinal fluid flow imaging in the meningeal hemorrhage]. Neurochirurgie 2006, 52:323-329. 10.1016/S0028-3770(06)71226-7, 17088712.
7. Brinker T, Seifert V, Stolke D. Acute changes in the dynamics of the cerebrospinal fluid system during experimental subarachnoid hemorrhage. Neurosurgery 1990, 27:369-372. 10.1227/00006123-199009000-00005, 2234329.
8. Schwab S, Schellinger P, Aschoff A, Albert F, Spranger M, Hacke W. [Epidural cerebrospinal fluid pressure measurement and therapy of intracranial hypertension in " malignant" middle cerebral artery infarct]. Nervenarzt 1996, 67:659-666. 10.1007/s001150050038, 8805111.
9. Minnerup J, Wersching H, Ringelstein EB, Heindel W, Niederstadt T, Schilling M, Schabitz WR, Kemmling A. Prediction of malignant middle cerebral artery infarction using computed tomography-based intracranial volume reserve measurements. Stroke 2011, 42:3403-3409. 10.1161/STROKEAHA.111.619734, 21903965.
10. Johanson C, Stopa E, Baird A, Sharma H. Traumatic brain injury and recovery mechanisms: peptide modulation of periventricular neurogenic regions by the choroid plexus-CSF nexus. J Neural Transm 2011, 118:115-133. 10.1007/s00702-010-0498-0, 3026679, 20936524.
11. Schmid Daners M, Knobloch V, Soellinger M, Boesiger P, Seifert B, Guzzella L, Kurtcuoglu V. Age-specific characteristics and coupling of cerebral arterial inflow and cerebrospinal fluid dynamics. PLoS One 2012, 7:e37502. 10.1371/journal.pone.0037502, 3364266, 22666360.
12. Stoquart-ElSankari S, Baledent O, Gondry-Jouet C, Makki M, Godefroy O, Meyer ME. Aging effects on cerebral blood and cerebrospinal fluid flows. J Cereb Blood Flow Metab 2007, 27:1563-1572. 10.1038/sj.jcbfm.9600462, 17311079.
13. Tripathi R. Tracing the bulk outflow route of cerebrospinal fluid by transmission and scanning electron microscopy. Brain Res 1974, 80:503-506. 10.1016/0006-8993(74)91033-6, 4214009.
14. Tripathi BJ, Tripathi RC. Vacuolar transcellular channels as a drainage pathway for cerebrospinal fluid. J Physiol 1974, 239:195-206. 1330945, 4369428.
15. Welch K, Friedman V. The cerebrospinal fluid valves. Brain 1960, 83:454-469. 10.1093/brain/83.3.454, 13784191.
16. Cserr HF, Harling-Berg CJ, Knopf PM. Drainage of brain extracellular fluid into blood and deep cervical lymph and its immunological significance. Brain Pathol 1992, 2:269-276. 10.1111/j.1750-3639.1992.tb00703.x, 1341962.
17. Zakharov A, Papaiconomou C, Koh L, Djenic J, Bozanovic-Sosic R, Johnston M. Integrating the roles of extracranial lymphatics and intracranial veins in cerebrospinal fluid absorption in sheep. Microvasc Res 2004, 67:96-104. 10.1016/j.mvr.2003.08.004, 14709407.
18. Kida S, Pantazis A, Weller RO. CSF drains directly from the subarachnoid space into nasal lymphatics in the rat. Anatomy, histology and immunological significance. Neuropathol Appl Neurobiol 1993, 19:480-488. 10.1111/j.1365-2990.1993.tb00476.x, 7510047.
19. Carare RO, Hawkes CA, Weller RO. Afferent and efferent immunological pathways of the brain. Anatomy, function and failure. Brain Behav Immun 2014, 36:9-14.
20. 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. 10.1186/1743-8454-1-2, 546409, 15679948.
21. Nagra G, Koh L, Zakharov A, Armstrong D, Johnston M. Quantification of cerebrospinal fluid transport across the cribriform plate into lymphatics in rats. Am J Physiol Regul Integr Comp Physiol 2006, 291:R1383-R1389. 10.1152/ajpregu.00235.2006, 16793937.
22. Johnston M, Zakharov A, Koh L, Armstrong D. Subarachnoid injection of Microfil reveals connections between cerebrospinal fluid and nasal lymphatics in the non-human primate. Neuropathol Appl Neurobiol 2005, 31:632-640. 10.1111/j.1365-2990.2005.00679.x, 16281912.
23. Boulton M, Young A, Hay J, Armstrong D, Flessner M, Schwartz M, Johnston M. Drainage of CSF through lymphatic pathways and arachnoid villi in sheep: measurement of 125I-albumin clearance. Neuropathol Appl Neurobiol 1996, 22:325-333. 10.1111/j.1365-2990.1996.tb01111.x, 8875467.
24. Boulton M, Flessner M, Armstrong D, Mohamed R, Hay J, Johnston M. Contribution of extracranial lymphatics and arachnoid villi to the clearance of a CSF tracer in the rat. Am J Physiol 1999, 276:R818-R823.
25. Boulton M, Flessner M, Armstrong D, Hay J, Johnston M. Lymphatic drainage of the CNS: effects of lymphatic diversion/ligation on CSF protein transport to plasma. Am J Physiol 1997, 272:R1613-R1619.
26. Silver I, Li B, Szalai J, Johnston M. Relationship between intracranial pressure and cervical lymphatic pressure and flow rates in sheep. Am J Physiol 1999, 277:R1712-R1717.
27. Mollanji R, Bozanovic-Sosic R, Zakharov A, Makarian L, Johnston MG. Blocking cerebrospinal fluid absorption through the cribriform plate increases resting intracranial pressure. Am J Physiol Regul Integr Comp Physiol 2002, 282:R1593-R1599.
28. Papaiconomou C, Zakharov A, Azizi N, Djenic J, Johnston M. Reassessment of the pathways responsible for cerebrospinal fluid absorption in the neonate. Childs Nerv Syst 2004, 20:29-36. 10.1007/s00381-003-0840-z, 14605840.
29. Welch K, Pollay M. The spinal arachnoid villi of the monkeys Cercopithecus aethiops sabaeus and Macaca irus. Anat Rec 1963, 145:43-48. 10.1002/ar.1091450107, 13999821.
30. Gomez DG, Chambers AA, Di Benedetto AT, Potts DG. The spinal cerebrospinal fluid absorptive pathways. Neuroradiology 1974, 8:61-66. 10.1007/BF00345037, 4140480.
31. Kido DK, Gomez DG, Pavese AM, Potts DG. Human spinal arachnoid villi and granulations. Neuroradiology 1976, 11:221-228. 10.1007/BF00328377, 980235.
32. Tubbs RS, Hansasuta A, Stetler W, Kelly DR, Blevins D, Humphrey R, Chua GD, Shoja MM, Loukas M, Oakes WJ. Human spinal arachnoid villi revisited: immunohistological study and review of the literature. J Neurosurg Spine 2007, 7:328-331. 10.3171/SPI-07/09/328, 17877268.
33. Marmarou A, Shulman K, LaMorgese J. Compartmental analysis of compliance and outflow resistance of the cerebrospinal fluid system. J Neurosurg 1975, 43:523-534. 10.3171/jns.1975.43.5.0523, 1181384.
34. Bozanovic-Sosic R, Mollanji R, Johnston MG. Spinal and cranial contributions to total cerebrospinal fluid transport. Am J Physiol Regul Integr Comp Physiol 2001, 281:R909-R916.
35. Edsbagge M, Tisell M, Jacobsson L, Wikkelso C. Spinal CSF absorption in healthy individuals. Am J Physiol Regul Integr Comp Physiol 2004, 287:R1450-R1455. 10.1152/ajpregu.00215.2004, 15308484.
36. Ritter S, Dinh TT. Progressive postnatal dilation of brain ventricles in spontaneously hypertensive rats. Brain Res 1986, 370:327-332. 10.1016/0006-8993(86)90488-9, 3708330.
37. Ritter S, Dinh TT, Stone S, Ross N. Cerebroventricular dilation in spontaneously hypertensive rats (SHRs) is not attenuated by reduction of blood pressure. Brain Res 1988, 450:354-359. 10.1016/0006-8993(88)91574-0, 3042092.
38. Murtha LA, McLeod DD, McCann SK, Pepperall D, Chung S, Levi CR, Calford MB, Spratt NJ. Short-duration hypothermia after ischemic stroke prevents delayed intracranial pressure rise. Int J Stroke 2013, doi:10.1111/ijs.12181.
39. Artru AA. Isoflurane does not increase the rate of CSF production in the dog. Anesthesiology 1984, 60:193-197. 10.1097/00000542-198403000-00004, 6696252.
40. Murtha L, McLeod D, Spratt N. Epidural intracranial pressure measurement in rats using a fiber-optic pressure transducer. J Vis Exp 2012, 62:e3689. doi:10,3791/3689.
41. McLeod D, Parsons M, Hood R, Hiles B, Allen J, McCann S, Murtha L, Calford M, Levi C, Spratt N. Perfusion computed tomography thresholds defining ischaemic penumbra and infarct core: studies in a rat stroke model. Int J Stroke 2013, doi: 10.1111/ijs.12147.
42. McLeod DD, Parsons MW, Levi CR, Beautement S, Buxton D, Roworth B, Spratt NJ. Establishing a rodent stroke perfusion computed tomography model. Int J Stroke 2011, 6:284-289. 10.1111/j.1747-4949.2010.00564.x, 21609409.
43. Chiu C, Miller MC, Caralopoulos IN, Worden MS, Brinker T, Gordon ZN, Johanson CE, Silverberg GD. Temporal course of cerebrospinal fluid dynamics and amyloid accumulation in the aging rat brain from three to thirty months. Fluids Barriers CNS 2012, 9:3. 10.1186/2045-8118-9-3, 3274479, 22269091.
44. 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. Sleep drives metabolite clearance from the adult brain. Science 2013, 342:373-377. 10.1126/science.1241224, 24136970.
45. Sykova E, Vorisek I, Antonova T, Mazel T, Meyer-Luehmann M, Jucker M, Hajek M, Ort M, Bures J. Changes in extracellular space size and geometry in APP23 transgenic mice: a model of Alzheimer's disease. Proc Natl Acad Sci U S A 2005, 102:479-484. 10.1073/pnas.0408235102, 544312, 15630088.
46. Al-Sarraf H, Philip L. Effect of hypertension on the integrity of blood brain and blood CSF barriers, cerebral blood flow and CSF secretion in the rat. Brain Res 2003, 975:179-188. 10.1016/S0006-8993(03)02632-5, 12763606.
47. Al-Sarraf H, Philip L. Increased brain uptake and CSF clearance of 14C-glutamate in spontaneously hypertensive rats. Brain Res 2003, 994:181-187. 10.1016/j.brainres.2003.09.034, 14642643.
48. Dunn LT. Raised intracranial pressure. J Neurol Neurosurg Psychiatry 2002, 73(Suppl 1):i23-i27. 1765599, 12185258.
49. Rangel Castilla L, Gopinath S, Robertson CS. Management of intracranial hypertension. Neurol Clin 2008, 26:521-541. x, 10.1016/j.ncl.2008.02.003, 2452989, 18514825.
50. Hawkins BE, Cowart JC, Parsley MA, Capra BA, Eidson KA, Hellmich HL, Dewitt DS, Prough DS. Effects of trauma, hemorrhage and resuscitation in aged rats. Brain Res 2013, 1496:28-35. 3569488, 23274538.
51. Ghersi-Egea JF, Finnegan W, Chen JL, Fenstermacher JD. Rapid distribution of intraventricularly administered sucrose into cerebrospinal fluid cisterns via subarachnoid velae in rat. Neuroscience 1996, 75:1271-1288. 10.1016/0306-4522(96)00281-3, 8938759.
52. Lai YL, Smith PM, Lamm WJ, Hildebrandt J. Sampling and analysis of cerebrospinal fluid for chronic studies in awake rats. J Appl Physiol 1983, 54:1754-1757.
53. Cserr HF. Physiology of the choroid plexus. Physiol Rev 1971, 51:273-311.
54. Cutler RW, Page L, Galicich J, Watters GV. Formation and absorption of cerebrospinal fluid in man. Brain 1968, 91:707-720. 10.1093/brain/91.4.707, 5304069.
55. Johanson CE, Duncan JA, Klinge PM, Brinker T, Stopa EG, Silverberg GD. Multiplicity of cerebrospinal fluid functions: New challenges in health and disease. Cerebrospinal Fluid Res 2008, 5:10. 10.1186/1743-8454-5-10, 2412840, 18479516.
56. Preston JE. Ageing choroid plexus-cerebrospinal fluid system. Microsc Res Tech 2001, 52:31-37. 10.1002/1097-0029(20010101)52:1<31::AID-JEMT5>3.0.CO;2-T, 11135446.
57. Redzic ZB, Preston JE, Duncan JA, Chodobski A, Szmydynger-Chodobska J. The choroid plexus-cerebrospinal fluid system: from development to aging. Curr Top Dev Biol 2005, 71:1-52.
58. Hochwald GM, Sahar A. Effect of spinal fluid pressure on cerebrospinal fluid formation. Exp Neurol 1971, 32:30-40. 10.1016/0014-4886(71)90162-2, 5095607.
59. Carey ME, Vela AR. Effect of systemic arterial hypotension on the rate of cerebrospinal fluid formation in dogs. J Neurosurg 1974, 41:350-355. 10.3171/jns.1974.41.3.0350, 4413096.
60. Snodgrass SR, Lorenzo AV. Temperature and cerebrospinal fluid production rate. Am J Physiol 1972, 222:1524-1527.
61. Paxinos G, Watson C. The rat brain in stereotaxic coordinates 1998, San Diego: Academic Press, 4.