Purpose
To investigate the biomechanical properties of the optic nerve sheath (i.e. fluid permeation across the meninges and tissue stiffness) at various CSF pressures. Such information is relevant to understanding ophthalmic changes associated with long-duration space flight (i.e. Visual Impairment and Intracranial Pressure syndrome; VIIP), thought to be largely due to cephalad fluid shifts causing altered ocular, cardiovascular, lymphatic and cerebrospinal fluid (CSF) pressures. The hypothesis is that increased CSF pressure drives connective tissue remodeling of the posterior eye and optic nerve sheath.
Methods
The meninges of fresh porcine eyes (n=10) was reflected to expose the optic nerve, which was truncated 3-4 mm posterior to the sclera. The meninges were repositioned leaving a “hollow” cylinder of connective tissue attached to the posterior sclera. The distal end was cannulated, sealed, and attached to a pressure control system that simulated CSF pressure changes. The anterior chamber of the eye was also cannulated for independent control of intraocular pressure (IOP). While IOP remained stable, a CCD camera recorded the meningeal diameter as the CSF pressure cycled between 7-50 mmHg. In a second set of experiments, the rate of fluid permeation across the meninges was recorded by observing the drainage of an elevated fluid reservoir connected to the meninges.
Results
Cyclic pressure-diameter curves showed a preconditioning effect, with repeatable behavior in cycles 4-6 (Figure). The meninges showed marked nonlinear stiffening, particularly at CSF pressures >15 mmHg. The tangent moduli extracted from these data were 318, 745, and 1273 kPa at CSF pressures of 7, 15 and 30 mmHg, respectively. Permeability experiments determined a flow rate of ~2ml/hr through the intact meninges at a driving pressure of 30mmHg, corresponding to a permeability of 7.34x10-5 ml/min/cm2/mmHg.
Conclusions
The meninges demonstrate biomechanical properties typical of other soft tissues, with nonlinear stiffening and appreciable hysteresis on pressure cycling. This tissue is surprisingly permeable, suggesting that there could be important CSF drainage through the meninges into the periorbital fat. These experimental measurements, extended to cadaveric eyes, will be critical in informing computational models aimed at identifying the pathophysiology of VIIP syndrome.
Keywords: 629 optic nerve •
519 extracellular matrix •
631 orbit