Breakdown of the meningeal barrier surrounding the intraorbital optic nerve after experimental subarachnoid hemorrhage

Abstract

Purpose: The intraorbital optic nerve sheath meninges contain a perineural subarachnoid space lined by meningeal cell layers and intercellular fibrous tissue. We sought to determine whether functional or structural characteristics, or both, of the optic nerve sheath are influenced by the increased intracranial pressure after the rupture of cerebral aneurysms.

Methods: We infused the great cisterns of cats with either x-ray contrast medium or autologous blood. The cisternal infusions were done under the experimental condition of a sudden 2.5-minute increase in intracranial pressure similar to that recorded after the rupture of cerebral aneurysms in humans.

Results: Digital subtraction radiographs of the optic nerves taken during the cisternal infusion of contrast medium at the start showed the opacification of the optic nerve subarachnoid space. After 2 minutes, the contrast medium leaked into the orbit, indicating the breakdown of the meningeal fluid barrier. Ultrastructural investigation of the optic nerve sheath after high-pressure cisternal infusions showed the arachnoid cell layers scattered. The flattened arachnoid cells displayed mainly intracellular and some intercellular, porelike openings. After infusion of blood into the great cistern, erythrocytes were found within porelike openings of the arachnoid cells.

Conclusions: The meningeal fluid barrier of the optic nerve sheath can be destroyed by pressure changes associated with subarachnoid hemorrhage. This disruption might be regarded as a natural optic nerve sheath fenestration that allows outflow of cerebrospinal fluid into the orbit to protect the optic nerve from increased intracranial pressure after aneurysmal rupture.