Skip to main content
Top
Published in: Fluids and Barriers of the CNS 1/2007

Open Access 01-12-2007 | Short paper

Possible role of the cavernous sinus veins in cerebrospinal fluid absorption

Authors: Miles Johnston, Dianna Armstrong, Lena Koh

Published in: Fluids and Barriers of the CNS | Issue 1/2007

Login to get access

Abstract

The purpose of this investigation was to enhance our understanding of cerebrospinal fluid (CSF) absorption pathways. To achieve this, Microfil (a coloured silastic material) was infused into the subarachnoid space (cisterna magna) of sheep post mortem, and the relevant tissues examined macroscopically and microscopically. The Microfil was taken up by an extensive network of extracranial lymphatic vessels in the olfactory turbinates. In addition however, Microfil also passed consistently through the dura at the base of the brain. Microfil was noted in the spaces surrounding the venous network that comprises the cavernous sinus, in the adventitia of the internal carotid arteries and adjacent to the pituitary gland. Additionally, Microfil was observed within the endoneurial spaces of the trigeminal nerve and in lymphatic vessels emerging from the epineurium of the nerve. These results suggest several unconventional pathways by which CSF may be removed from the subarachnoid space. The movement of CSF to locations external to the cranium via these routes may lead to its absorption into veins and lymphatics outside of the skull. The physiological importance of these pathways requires further investigation.
Appendix
Available only for authorised users
Literature
1.
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
2.
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
3.
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
4.
go back to reference Boulton M, Flessner M, Armstrong D, Hay J, Johnston M: Determination of volumetric cerebrospinal fluid absorption into extracranial lymphatics in sheep. Am J Physiol. 1998, 274: R88-R96.PubMed Boulton M, Flessner M, Armstrong D, Hay J, Johnston M: Determination of volumetric cerebrospinal fluid absorption into extracranial lymphatics in sheep. Am J Physiol. 1998, 274: R88-R96.PubMed
5.
go back to reference Mollanji R, Bozanovic-Sosic R, Silver I, Li B, Kim C, Midha R, Johnston M: Intracranial pressure accommodation is impaired by blocking pathways leading to extracranial lymphatics. Am J Physiol Regul Integr Comp Physiol. 2001, 280: R1573-R1581.PubMed Mollanji R, Bozanovic-Sosic R, Silver I, Li B, Kim C, Midha R, Johnston M: Intracranial pressure accommodation is impaired by blocking pathways leading to extracranial lymphatics. Am J Physiol Regul Integr Comp Physiol. 2001, 280: R1573-R1581.PubMed
6.
go back to reference Papaiconomou C, Bozanovic-Sosic R, Zakharov A, Johnston M: Does neonatal cerebrospinal fluid absorption occur via arachnoid projections or extracranial lymphatics?. Am J Physiol Regul Integr Comp Physiol. 2002, 283: R869-R876.CrossRefPubMed Papaiconomou C, Bozanovic-Sosic R, Zakharov A, Johnston M: Does neonatal cerebrospinal fluid absorption occur via arachnoid projections or extracranial lymphatics?. Am J Physiol Regul Integr Comp Physiol. 2002, 283: R869-R876.CrossRefPubMed
7.
go back to reference Zakharov A, Papaiconomou C, Djenic J, Midha R, Johnston M: Lymphatic cerebrospinal fluid absorption pathways in neonatal sheep revealed by subarachnoid injection of Microfil. Neuropathol Appl Neurobiol. 2003, 29: 563-573. 10.1046/j.0305-1846.2003.00508.x.CrossRefPubMed Zakharov A, Papaiconomou C, Djenic J, Midha R, Johnston M: Lymphatic cerebrospinal fluid absorption pathways in neonatal sheep revealed by subarachnoid injection of Microfil. Neuropathol Appl Neurobiol. 2003, 29: 563-573. 10.1046/j.0305-1846.2003.00508.x.CrossRefPubMed
8.
go back to reference Kawase T, van Loveren H, Keller JT, Tew JM: Meningeal architecture of the cavernous sinus: clinical and surgical implications. Neurosurgery. 1996, 39: 527-534. 10.1097/00006123-199609000-00019.PubMed Kawase T, van Loveren H, Keller JT, Tew JM: Meningeal architecture of the cavernous sinus: clinical and surgical implications. Neurosurgery. 1996, 39: 527-534. 10.1097/00006123-199609000-00019.PubMed
9.
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
10.
go back to reference Foldi M, Gellert A, Kozma M, Poberai M, Zoltan OT, Csanda E: New contributions to the anatomical connections of the brain and the lymphatic system. Acta Anat (Basel). 1966, 64: 498-505.CrossRef Foldi M, Gellert A, Kozma M, Poberai M, Zoltan OT, Csanda E: New contributions to the anatomical connections of the brain and the lymphatic system. Acta Anat (Basel). 1966, 64: 498-505.CrossRef
11.
go back to reference Andres KH, von During M, Muszynski K, Schmidt RF: Nerve fibres and their terminals of the dura mater encephali of the rat. Anat Embryol (Berl). 1987, 175: 289-301. 10.1007/BF00309843.CrossRef Andres KH, von During M, Muszynski K, Schmidt RF: Nerve fibres and their terminals of the dura mater encephali of the rat. Anat Embryol (Berl). 1987, 175: 289-301. 10.1007/BF00309843.CrossRef
12.
go back to reference Rodriguez-Peralta LA: The role of the meningeal tissues in the hematoencephalic barrier. J Comp Neurol. 1957, 107: 455-473. 10.1002/cne.901070308.CrossRefPubMed Rodriguez-Peralta LA: The role of the meningeal tissues in the hematoencephalic barrier. J Comp Neurol. 1957, 107: 455-473. 10.1002/cne.901070308.CrossRefPubMed
13.
go back to reference Killer HE, Laeng HR, Groscurth P: Lymphatic capillaries in the meninges of the human optic nerve. J Neuroophthalmol. 1999, 19: 222-228.PubMed Killer HE, Laeng HR, Groscurth P: Lymphatic capillaries in the meninges of the human optic nerve. J Neuroophthalmol. 1999, 19: 222-228.PubMed
14.
go back to reference De La Motte DJ: Removal of horseradish peroxidase and fluorescein-labelled dextran from CSF spaces of rabbit optic nerve. A light and electron microscope study. Exp Eye Res. 1978, 27: 585-594. 10.1016/0014-4835(78)90143-4.CrossRefPubMed De La Motte DJ: Removal of horseradish peroxidase and fluorescein-labelled dextran from CSF spaces of rabbit optic nerve. A light and electron microscope study. Exp Eye Res. 1978, 27: 585-594. 10.1016/0014-4835(78)90143-4.CrossRefPubMed
15.
go back to reference Holtz E, Michelet AA, Jacobsen T: Absorption after subarachnoid and subdural administration of iohexol, 51Cr-EDTA, and 125I-albumin to rabbits. Am J Neuroradiol. 1983, 4: 338-341.PubMed Holtz E, Michelet AA, Jacobsen T: Absorption after subarachnoid and subdural administration of iohexol, 51Cr-EDTA, and 125I-albumin to rabbits. Am J Neuroradiol. 1983, 4: 338-341.PubMed
16.
go back to reference Foldi M, Csanda G, Simon M, Obal F, Schneider I, Dobranovics I, Zoltan OT, Kozma M, Poberai M: Lymphogenic haemangiography "prelymphatic" pathways in the wall of cerebral and cervical blood vessels. Angiologica. 1968, 5: 250-262.PubMed Foldi M, Csanda G, Simon M, Obal F, Schneider I, Dobranovics I, Zoltan OT, Kozma M, Poberai M: Lymphogenic haemangiography "prelymphatic" pathways in the wall of cerebral and cervical blood vessels. Angiologica. 1968, 5: 250-262.PubMed
17.
go back to reference Casley-Smith JR, Foldi-Borsok E, Foldi M: The prelymphatic pathways of the brain as revealed by cervical lymphatic obstruction and the passage of particles. Br J Exp Pathol. 1976, 57: 179-188.PubMedCentralPubMed Casley-Smith JR, Foldi-Borsok E, Foldi M: The prelymphatic pathways of the brain as revealed by cervical lymphatic obstruction and the passage of particles. Br J Exp Pathol. 1976, 57: 179-188.PubMedCentralPubMed
18.
go back to reference Wang HJ, Casley-Smith JR: Drainage of the prelymphatics of the brain via the adventitia of the vertebral artery. Acta Anat (Basel). 1989, 134: 67-71.CrossRef Wang HJ, Casley-Smith JR: Drainage of the prelymphatics of the brain via the adventitia of the vertebral artery. Acta Anat (Basel). 1989, 134: 67-71.CrossRef
19.
go back to reference Bradbury MW, Cserr HF: Drainage of cerebral interstitial fluid and of cerebrospinal fluid into lymphatics. Experimental Biology of the Lymphatic Circulation. Edited by: Johnston M. 1985, New York, Elsevier Science Publishers, 355-349. Bradbury MW, Cserr HF: Drainage of cerebral interstitial fluid and of cerebrospinal fluid into lymphatics. Experimental Biology of the Lymphatic Circulation. Edited by: Johnston M. 1985, New York, Elsevier Science Publishers, 355-349.
20.
go back to reference Koh L, Zakharov A, Johnston M: Integration of the subarachnoid space and lymphatics: is it time to embrace a new concept of cerebrospinal fluid absorption?. Cerebrospinal Fluid Res. 2005, 2: 6-10.1186/1743-8454-2-6.PubMedCentralCrossRefPubMed Koh L, Zakharov A, Johnston M: Integration of the subarachnoid space and lymphatics: is it time to embrace a new concept of cerebrospinal fluid absorption?. Cerebrospinal Fluid Res. 2005, 2: 6-10.1186/1743-8454-2-6.PubMedCentralCrossRefPubMed
21.
go back to reference Manzo RP, Gomez DG, Potts DG: Cerebrospinal fluid absorption in the rabbit. Inner ear pathways. Acta Otolaryngol. 1990, 109: 389-396.CrossRefPubMed Manzo RP, Gomez DG, Potts DG: Cerebrospinal fluid absorption in the rabbit. Inner ear pathways. Acta Otolaryngol. 1990, 109: 389-396.CrossRefPubMed
22.
go back to reference Nakao Y, Tabuchi T, Sakihama N, Nakajima S: Extracellular fluid pathway inside the facial nerve fascicles. Ann Otol Rhinol Laryngol. 1997, 106: 503-505.CrossRefPubMed Nakao Y, Tabuchi T, Sakihama N, Nakajima S: Extracellular fluid pathway inside the facial nerve fascicles. Ann Otol Rhinol Laryngol. 1997, 106: 503-505.CrossRefPubMed
23.
go back to reference Myers RR, Rydevik BL, Heckman HM, Powell HC: Proximodistal gradient in endoneurial fluid pressure. Exp Neurol. 1988, 102: 368-370. 10.1016/0014-4886(88)90233-6.CrossRefPubMed Myers RR, Rydevik BL, Heckman HM, Powell HC: Proximodistal gradient in endoneurial fluid pressure. Exp Neurol. 1988, 102: 368-370. 10.1016/0014-4886(88)90233-6.CrossRefPubMed
24.
go back to reference Takeda T, Takeuchi S, Kishimoto S, Saito H: Interstitial fluid pressure in the facial nerve: relationship between facial nerve pressure and cerebrospinal fluid pressure. Am J Otolaryngol. 1989, 10: 345-350. 10.1016/0196-0709(89)90111-7.CrossRefPubMed Takeda T, Takeuchi S, Kishimoto S, Saito H: Interstitial fluid pressure in the facial nerve: relationship between facial nerve pressure and cerebrospinal fluid pressure. Am J Otolaryngol. 1989, 10: 345-350. 10.1016/0196-0709(89)90111-7.CrossRefPubMed
Metadata
Title
Possible role of the cavernous sinus veins in cerebrospinal fluid absorption
Authors
Miles Johnston
Dianna Armstrong
Lena Koh
Publication date
01-12-2007
Publisher
BioMed Central
Published in
Fluids and Barriers of the CNS / Issue 1/2007
Electronic ISSN: 2045-8118
DOI
https://doi.org/10.1186/1743-8454-4-3

Other articles of this Issue 1/2007

Fluids and Barriers of the CNS 1/2007 Go to the issue