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Published in: Fluids and Barriers of the CNS 1/2014

Open Access 01-12-2014 | Research

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

Authors: Lucy A Murtha, Qing Yang, Mark W Parsons, Christopher R Levi, Daniel J Beard, Neil J Spratt, Damian D McLeod

Published in: Fluids and Barriers of the CNS | Issue 1/2014

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Abstract

Background

Many aspects of CSF dynamics are poorly understood due to the difficulties involved in quantification and visualization. In particular, there is debate surrounding the route of CSF drainage. Our aim was to quantify CSF flow, volume, and drainage route dynamics in vivo in young and aged spontaneously hypertensive rats (SHR) using a novel contrast-enhanced computed tomography (CT) method.

Methods

ICP was recorded in young (2–5 months) and aged (16 months) SHR. Contrast was administered into the lateral ventricles bilaterally and sequential CT imaging was used to visualize the entire intracranial CSF system and CSF drainage routes. A customized contrast decay software module was used to quantify CSF flow at multiple locations.

Results

ICP was significantly higher in aged rats than in young rats (11.52 ± 2.36 mmHg, versus 7.04 ± 2.89 mmHg, p = 0.03). Contrast was observed throughout the entire intracranial CSF system and was seen to enter the spinal canal and cross the cribriform plate into the olfactory mucosa within 9.1 ± 6.1 and 22.2 ± 7.1 minutes, respectively. No contrast was observed adjacent to the sagittal sinus. There were no significant differences between young and aged rats in either contrast distribution times or CSF flow rates. Mean flow rates (combined young and aged) were 3.0 ± 1.5 μL/min at the cerebral aqueduct; 3.5 ± 1.4 μL/min at the 3rd ventricle; and 2.8 ± 0.9 μL/min at the 4th ventricle. Intracranial CSF volumes (and as percentage total brain volume) were 204 ± 97 μL (8.8 ± 4.3%) in the young and 275 ± 35 μL (10.8 ± 1.9%) in the aged animals (NS).

Conclusions

We have demonstrated a contrast-enhanced CT technique for measuring and visualising CSF dynamics in vivo. These results indicate substantial drainage of CSF via spinal and olfactory routes, but there was little evidence of drainage via sagittal sinus arachnoid granulations in either young or aged animals. The data suggests that spinal and olfactory routes are the primary routes of CSF drainage and that sagittal sinus arachnoid granulations play a minor role, even in aged rats with higher ICP.
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Literature
1.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
2.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
3.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
4.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
5.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
6.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
7.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
8.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
9.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
10.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
11.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
12.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
13.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
15.
go back to reference Welch K, Friedman V: The cerebrospinal fluid valves. Brain. 1960, 83: 454-469. 10.1093/brain/83.3.454.CrossRefPubMed Welch K, Friedman V: The cerebrospinal fluid valves. Brain. 1960, 83: 454-469. 10.1093/brain/83.3.454.CrossRefPubMed
16.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
17.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
18.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
19.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
20.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
21.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
22.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
23.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
24.
go back to reference 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.PubMed 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.PubMed
25.
go back to reference 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.PubMed 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.PubMed
26.
go back to reference 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.PubMed 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.PubMed
27.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
28.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
29.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
30.
go back to reference Gomez DG, Chambers AA, Di Benedetto AT, Potts DG: The spinal cerebrospinal fluid absorptive pathways. Neuroradiology. 1974, 8: 61-66. 10.1007/BF00345037.CrossRefPubMed Gomez DG, Chambers AA, Di Benedetto AT, Potts DG: The spinal cerebrospinal fluid absorptive pathways. Neuroradiology. 1974, 8: 61-66. 10.1007/BF00345037.CrossRefPubMed
31.
go back to reference Kido DK, Gomez DG, Pavese AM, Potts DG: Human spinal arachnoid villi and granulations. Neuroradiology. 1976, 11: 221-228. 10.1007/BF00328377.CrossRefPubMed Kido DK, Gomez DG, Pavese AM, Potts DG: Human spinal arachnoid villi and granulations. Neuroradiology. 1976, 11: 221-228. 10.1007/BF00328377.CrossRefPubMed
32.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
33.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
34.
go back to reference 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.PubMed 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.PubMed
35.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
36.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
37.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
38.
go back to reference 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 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.
go back to reference Artru AA: Isoflurane does not increase the rate of CSF production in the dog. Anesthesiology. 1984, 60: 193-197. 10.1097/00000542-198403000-00004.CrossRefPubMed Artru AA: Isoflurane does not increase the rate of CSF production in the dog. Anesthesiology. 1984, 60: 193-197. 10.1097/00000542-198403000-00004.CrossRefPubMed
40.
go back to reference 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 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.
go back to reference 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 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.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
43.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
44.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
45.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
46.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
47.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
49.
go back to reference Rangel Castilla L, Gopinath S, Robertson CS: Management of intracranial hypertension. Neurol Clin. 2008, 26: 521-541. 10.1016/j.ncl.2008.02.003. xCrossRefPubMed Rangel Castilla L, Gopinath S, Robertson CS: Management of intracranial hypertension. Neurol Clin. 2008, 26: 521-541. 10.1016/j.ncl.2008.02.003. xCrossRefPubMed
50.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
51.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
52.
go back to reference 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.PubMed 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.PubMed
53.
go back to reference Cserr HF: Physiology of the choroid plexus. Physiol Rev. 1971, 51: 273-311.PubMed Cserr HF: Physiology of the choroid plexus. Physiol Rev. 1971, 51: 273-311.PubMed
54.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
55.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
56.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
57.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
58.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
59.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
60.
go back to reference Snodgrass SR, Lorenzo AV: Temperature and cerebrospinal fluid production rate. Am J Physiol. 1972, 222: 1524-1527.PubMed Snodgrass SR, Lorenzo AV: Temperature and cerebrospinal fluid production rate. Am J Physiol. 1972, 222: 1524-1527.PubMed
61.
go back to reference Paxinos G, Watson C: The rat brain in stereotaxic coordinates. 1998, San Diego: Academic Press, 4 Paxinos G, Watson C: The rat brain in stereotaxic coordinates. 1998, San Diego: Academic Press, 4
Metadata
Title
Cerebrospinal fluid is drained primarily via the spinal canal and olfactory route in young and aged spontaneously hypertensive rats
Authors
Lucy A Murtha
Qing Yang
Mark W Parsons
Christopher R Levi
Daniel J Beard
Neil J Spratt
Damian D McLeod
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Fluids and Barriers of the CNS / Issue 1/2014
Electronic ISSN: 2045-8118
DOI
https://doi.org/10.1186/2045-8118-11-12

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