Abstract
Purpose
The optic nerve (ON) is an extension of the central nervous system via the optic canal to the orbital cavity. It is accompanied by meninges whose arachnoid layer is in continuity with that of the chiasmatic cistern. This arachnoid layer is extended along the ON, delimiting a subarachnoid space (SAS) around the ON. Not all forms of chronic intracranial hypertension (ICH) present papilledema. The latter is sometimes asymmetric, unilateral, or absent. The radiological signs of optic nerve sheath (ONS) dilation, in magnetic resonance imaging, are inconsistent or difficult to interpret. The objective of this study was to analyze the anatomy, the constitution, and the variability of the SAS around the ON in its intraorbital segment to improve the understanding of the pathophysiologic mechanism of asymmetric or unilateral or absent papilledema in certain ICH.
Methods
The study was carried out on nine cadaveric specimens. In four embalmed specimens, macroscopic analysis of the SAS of the ONS were performed, with description about density of the arachnoid trabecular meshwork in three distinct areas (bulbar segment, mid-orbital segment and the precanal segment). In three other embalmed specimens, after staining of SAS by methylene blue (MB), we performed macroscopic analysis of MB progression in the SAS of the ONS. Then, in two non-embalmed specimens, light and electron microscopy (EM) analysis were also done.
Results
On the macroscopic level, after staining of SAS, we found in all cases that MB progressed on 16 mm average throughout the SAS of the ONS without reaching the papilla. In four embalmed specimens, in the SAS of the ONS, the density of the arachnoid trabecular meshwork showed inter-individual variability (100%) and intra-individual variability with bilateral variability (50%) and/or variability within the same ONS (88%). On the microscopic level, the arachnoid trabeculae of the ONS are composed of dense connective tissue. The EM perfectly depicted its composition which is mainly of collagen fibers of parallel orientation.
Conclusion
The variability of the SAS around the ONS probably impacts the symmetrical or asymmetrical nature of papilledema in ICH.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Banerjee M, Aalok SP, Vibha D (2020) Unilateral papilledema in idiopathic intracranial hypertension: a rare entity. Eur J Ophthalmol. https://doi.org/10.1177/1120672120969041
Bidot S, Bruce BB, Saindane AM, Newman NJ, Biousse V (2015) Asymmetric papilledema in idiopathic intracranial hypertension. J Neuroophthalmol 35:31–36. https://doi.org/10.1097/WNO.0000000000000205
Francois P, Lescanne E, Velut S (2011) The dural sheath of the optic nerve: descriptive anatomy and surgical applications. In: Pickard JD, Akalan N, Benes V, Di Rocco C, Dolenc VV, Antunes JL, Schramm J, Sindou M (eds) Advances and technical standards in neurosurgery. Springer Vienna, Vienna, pp 187–198
Friedman DI, Liu GT, Digre KB (2013) Revised diagnostic criteria for the pseudotumor cerebri syndrome in adults and children. Neurology 81:1159–1165. https://doi.org/10.1212/WNL.0b013e3182a55f17
Geeraerts T, Newcombe VF, Coles JP, Abate M, Perkes IE, Hutchinson PJ, Outtrim JG, Chatfield DA, Menon DK (2008) Use of T2-weighted magnetic resonance imaging of the optic nerve sheath to detect raised intracranial pressure. Crit Care 12:R114. https://doi.org/10.1186/cc7006
Hayreh SS (1968) Pathogenesis of oedema of the optic disc. Doc Ophthalmol 24:289–411. https://doi.org/10.1007/BF02550944
Hayreh SS (2016) Pathogenesis of optic disc edema in raised intracranial pressure. Prog Retin Eye Res 50:108–144. https://doi.org/10.1016/j.preteyeres.2015.10.001
Huna-Baron R, Landau K, Rosenberg M, Warren FA, Kupersmith MJ (2001) Unilateral swollen disc due to increased intracranial pressure. Neurology 56:1588–1590. https://doi.org/10.1212/WNL.56.11.1588
Jaggi GP, Harlev M, Ziegler U, Dotan S, Miller NR, Killer HE (2010) Cerebrospinal fluid segregation optic neuropathy: an experimental model and a hypothesis. Br J Ophthalmol 94:1088–1093. https://doi.org/10.1136/bjo.2009.171660
Jayatilaka ADP. A note on arachnoid villi in relation to human optic nerves. 3
Killer HE (1999) Lymphatic capillaries in the meninges of the human optic nerve. J Neuro-ophtalmol 19(4):222–228
Killer HE (2003) Architecture of arachnoid trabeculae, pillars, and septa in the subarachnoid space of the human optic nerve: anatomy and clinical considerations. Br J Ophthalmol 87:777–781. https://doi.org/10.1136/bjo.87.6.777
Killer HE, Jaggi GP, Flammer J, Miller NR, Huber AR (2006) The optic nerve: a new window into cerebrospinal fluid composition? Brain 129:1027–1030. https://doi.org/10.1093/brain/awl045
Killer HE, Jaggi GP, Flammer J, Miller NR, Huber AR, Mironov A (2007) Cerebrospinal fluid dynamics between the intracranial and the subarachnoid space of the optic nerve. Is it always bidirectional? Brain 130:514–520. https://doi.org/10.1093/brain/awl324
Klinge PM, McElroy A, Donahue JE, Brinker T, Gokaslan ZL, Beland MD (2021) Abnormal spinal cord motion at the craniocervical junction in hypermobile Ehlers–Danlos patients. J Neurosurg Spine 35:18–24. https://doi.org/10.3171/2020.10.SPINE201765
Liu D, Kahn M (1993) Measurement and relationship of subarachnoid pressure of the optic nerve to intracranial pressures in fresh cadavers. Am J Ophthalmol 116:548–556. https://doi.org/10.1016/S0002-9394(14)73195-2
Mienaltowski MJ, Birk DE (2014) Structure, physiology, and biochemistry of collagens. In: Halper J (ed) Progress in heritable soft connective tissue diseases. Springer Netherlands, Dordrecht, pp 5–29
Passi N, Degnan AJ, Levy LM (2013) MR imaging of papilledema and visual pathways: effects of increased intracranial pressure and pathophysiologic mechanisms. AJNR Am J Neuroradiol 34:919–924. https://doi.org/10.3174/ajnr.A3022
Pircher A, Montali M, Pircher J, Berberat J, Remonda L, Killer HE (2018) Perioptic cerebrospinal fluid dynamics in idiopathic intracranial hypertension. Front Neurol. https://doi.org/10.3389/fneur.2018.00506
Selhorst J, Chen Y (2009) The optic nerve. Semin Neurol 29:029–035. https://doi.org/10.1055/s-0028-1124020
Tsutsumi S, Ono H, Ishii H (2021) Hyperintense areas in the intraorbital optic nerve evaluated by T2-weighted magnetic resonance imaging: a glymphatic pathway? Surg Radiol Anat 43:1273–1278. https://doi.org/10.1007/s00276-020-02649-7
Watanabe A, Kinouchi H, Horikoshi T, Uchida M, Ishigame K (2008) Effect of intracranial pressure on the diameter of the optic nerve sheath. JNS 109:255–258. https://doi.org/10.3171/JNS/2008/109/8/0255
Author information
Authors and Affiliations
Contributions
Conception and design: AD, DL. Dissection and acquisition of data: AD. Analysis and interpretation of data: AD, VJ, DL. Drafting the article: AD. Critically revising the article: VJ, DL, MS, LLP. Reviewed submitted version of manuscript: AD.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest. Bordeaux Imaging Center has received research grants from Laboratory Anatomy of Bordeaux to finance EM analyzes.
Ethical approval
All procedures performed in study were in accordance with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Durouchoux, A., Liguoro, D., Sesay, M. et al. Subarachnoid space of the optic nerve sheath and intracranial hypertension: a macroscopic, light and electron microscopic study. Surg Radiol Anat 44, 759–766 (2022). https://doi.org/10.1007/s00276-022-02948-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00276-022-02948-1