Joel E. Pessa
Abstract
How cerebrospinal fluid (CSF) drains from the human brain is of paramount importance to cerebral health and physiology. Obstructed CSF drainage results in increased intra-cranial pressure and a predictable cascade of events including dilated cerebral ventricles and ultimately cell death. The current and accepted model of CSF drainage in humans suggests CSF drains from the subarachnoid space into the sagittal sinus vein. Here we identify a new structure in the sagittal sinus of the human brain by anatomic cadaver dissection. The CSF canalicular system is a series of channels on either side of the sagittal sinus vein that communicate with subarachnoid cerebrospinal fluid via Virchow-Robin spaces. Fluorescent injection confirms that these channels are patent and that flow occurs independent of the venous system. Fluoroscopy identified flow from the sagittal sinus to the cranial base. We verify our previous identification of CSF channels in the neck that travel from the cranial base to the subclavian vein. Together, this information suggests a novel path for CSF drainage of the human brain that may represent the primary route for CSF recirculation. These findings have implications for basic anatomy, surgery, and neuroscience, and highlight the continued importance of gross anatomy to medical research and discovery.
Introduction
How cerebrospinal fluid (CSF) drains from the human brain is of paramount importance to cerebral health and physiology. Obstructed CSF drainage results in increased intra-cranial pressure and a predictable cascade of events including dilated cerebral ventricles (hydrocephalus) and cell death [1, 2]. This paper identifies a new structure in the sagittal sinus of the human brain for CSF drainage, and confirms our previous findings of a CSF system in the neck. Together, this work suggests a novel path for CSF drainage of the human brain that could represent the primary path for CSF recirculation.
Materials and methods
Fresh cadaver dissections (not embalmed) were performed under institutional guidelines. The IRB committee reviewed this work and agreed that it does not require IRB approval or oversight. Seven (N = 7) dissections were performed in 5 male and 2 female cadavers. Ages ranged from 40–92 years (mean 82.5). The sagittal sinus was dissected to identify the bilateral CSF canalicular system, and photographs were obtained in selected specimens (Canon EOS 6D 50mm macro lens, Canon USA, Melville, NY). Fluoroscopy was performed after the CSF canalicular system was intubated with 0.25 mm silastic tubing (WPI, Sarasota, Florida) and injected with 0.2 mls of OmnipaqueTM (iohexol, GE Healthcare, Chicago, Illinois). The CSF channels in the sagittal sinus were injected in 1 specimen using 1–5μ fluorescent polymer spheres (CosphericTM, Santa Barbara, CA) after intubation with 22/24 gauge IV catheter (Baxter Healthcare Corporation, Deerfield, Illinois) and photographed under ambient/UV light. Neck dissections confirmed the anatomy of the CSF system in the neck in each specimen. One cervical biopsy was submitted for immunohistochemistry by 2-step indirect immunohistochemistry (IHC) for LYVE-1, D2-40, CD105, and F-actin (Sigma Aldrich, St. Louis, Missouri), and by direct IHC for the type-3 neurofilament protein vimentin (vimentin cy-3; Sigma Aldrich, St. Louis, Missouri) [15].
Results
Craniotomy exposed the dura and the midline venous sagittal sinus (Fig 3). After the sagittal sinus was opened, blood was evacuated to identify CSF channels located on either side of the venous sagittal sinus (Figs 4 and 5). A cross-section view shows the location of CSF channels relative to the venous sinus (Fig 6). CSF channels exist as a plexus that are located posteriorly and on either side of the venous system (Fig 7). Dissection identified the CSF system in all specimens.
Discussion
The identification of the CSF canalicular system has implications for basic anatomy, surgery, and neuroscience. It redefines the anatomy of the sagittal sinus. The definition of what structures travel in the carotid sheath could be amended to include the terminal CSF drainage of the brain [23]. The observation of retrograde fill of the arachnoid meninges will require further study to identify potential CSF channels in that layer. Sappey’s rule may need to be amended if further molecular analysis concludes that CSF channels are distinct from lymphatics and blood vessels [24].
Conclusion
This paper identifies a novel anatomical path for CSF drainage of the human brain. The identification of the CSF canalicular system has implications for anatomy, surgery, and neuroscience, and highlights the continued importance of gross anatomy to medical research and discovery.
Acknowledgments
The author thanks the donors of the UTSW Willed Body Program and their families. Without their generous gift this research would not be possible.
The author thanks the entire staff of the UTSW Willed Body Program for their help on this and all of our anatomical projects.
The author acknowledges Ronald M. Howorth MD’s help in validating this model and performing the fluorescence injection and imaging.
Citation: Pessa JE (2023) Identification of a novel path for cerebrospinal fluid (CSF) drainage of the human brain. PLoS ONE 18(5): e0285269. https://doi.org/10.1371/journal.pone.0285269
Editor: Alvan Ukachukwu, Duke University Medical Center: Duke University Hospital, UNITED STATES
Received: January 13, 2023; Accepted: April 18, 2023; Published: May 4, 2023
Copyright: © 2023 Joel E. Pessa. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The DATA is included within the paper.
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
