Interplay between intraocular and intracranial pressure effects on the optic nerve head in vivo

Zhu, Ziyi; Waxman, Susannah; Wang, Bo; Wallace, Jacob; Schmitt, Samantha; Tyler-Kabara, Elizabeth C.; Ishikawa, Hiroshi; Schuman, Joel S.; Smith, Matthew A.; Wollstein, Gadi; Sigal, Ian A.

doi:10.1016/j.exer.2021.108809

Cited by 13 publications

(14 citation statements)

References 68 publications

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“…In a particularly relevant study, Zhu and co-workers reported the LC deformation in NHPs subjected to independent manometric manipulation of IOP and CSFP. 92 They reported that CSFP elevation displaced the LC anteriorly by 10 µm at baseline IOP but the LC displaced 7 µm posteriorly at high IOP; these results are somewhat counterintuitive, although the relatively small changes were of the same magnitude as those we report herein. Similar magnitude LC deformations results were reported for IOP elevations at baseline and elevated CSFP.…”

Section: Discussioncontrasting

confidence: 46%

“…ALSD is one of the key biomarkers of glaucomatous optic neuropathy 97 because experimental studies have shown that LC displacement occurs at an early stage of the disease, 98 , 99 and may precede the retinal nerve fiber layer change as detected by OCT. 100 CSFP and IOP elevation increased the average and maximum ALSD by 4.67 µm and 11.30 µm, respectively, that is in good agreement with in vivo measurements in monkeys (7 µm). 54 …”

Section: Discussionmentioning

confidence: 99%

“…The role of simultaneous changes in IOP and CSFP 42 – 48 on ONH biomechanics has been studied both experimentally and computationally. 49 – 54 However, these studies considered the neural and connective tissues in the laminar region as a single homogenous material. Hence, little is known about how TLP alteration with change in body position affects the biomechanics of the LC beams themselves and the interspersed laminar NT.…”

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confidence: 99%

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Relative Contributions of Intraocular and Cerebrospinal Fluid Pressures to the Biomechanics of the Lamina Cribrosa and Laminar Neural Tissues

Karimi

Razaghi

Rahmati

et al. 2022

Invest. Ophthalmol. Vis. Sci.

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Purpose The laminar region of the optic nerve head (ONH), thought to be the site of damage to the retinal ganglion cell axons in glaucoma, is continuously loaded on its anterior and posterior surfaces by dynamic intraocular pressure (IOP) and orbital cerebrospinal fluid pressure (CSFP), respectively. Thus, translaminar pressure (TLP; TLP = IOP-CSFP) has been proposed as a glaucoma risk factor. Methods Three eye-specific finite element models of the posterior human eye were constructed, including full 3D microstructures of the load-bearing lamina cribrosa (LC) with interspersed laminar neural tissues (NTs), and heterogeneous, anisotropic, hyperelastic material formulations for the surrounding peripapillary sclera and adjacent pia. ONH biomechanical responses were simulated using three combinations of IOP and CSFP loadings consistent with posture change from sitting to supine. Results Results show that tensile, compressive, and shear stresses and strains in the ONH were higher in the supine position compared to the sitting position ( P < 0.05). In addition, LC beams bear three to five times more TLP-driven stress than interspersed laminar NT, whereas laminar NT exhibit three to five times greater strain than supporting LC ( P < 0.05). Compared with CSFP, IOP drove approximately four times greater stress and strain in the LC, NT, and peripapillary sclera, normalized per mm Hg pressure change. In addition, IOP drove approximately three-fold greater scleral canal expansion and anterior-posterior laminar deformation than CSFP per mm Hg ( P < 0.05). Conclusions Whereas TLP has been hypothesized to play a prominent role in ONH biomechanics, the IOP and CSFP effects are not equivalent, as IOP-driven stress, strain, and deformation play a more dominant role than CSFP effects.

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Section: Discussioncontrasting

confidence: 46%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Relative Contributions of Intraocular and Cerebrospinal Fluid Pressures to the Biomechanics of the Lamina Cribrosa and Laminar Neural Tissues

Karimi

Razaghi

Rahmati

et al. 2022

Invest. Ophthalmol. Vis. Sci.

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“…Twenty-six years later, Zhao et al used the electroretinogram to measure changes in retinal function when varying IOP in rats with normal ICP compared with reduced ICP, and found a larger TLPG resulted in worse retinal function (11). Most recently, Zhu et al conducted an in vivo study of monkeys using optical coherence tomography to image and quantify real-time deformations of the LC, and found that lowering ICP resulted in larger amplitude bowing of the LC in response to IOP variations (12). Further evidence of a relationship of optic nerve cupping related to changes in CSF pressure and flow dynamics is highlighted by works by Gallina and colleagues that examined the development of NTG in patients with shunttreated normal pressure hydrocephalus (13).…”

Section: Introductionmentioning

confidence: 99%

Problems in CSF and Ophthalmic Disease Research

Machiele¹,

Frankfort²,

Killer³

et al. 2022

Front. Ophthalmol.

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There has been significant interest and progress in the understanding of cerebrospinal fluid pressure and its relationship to glaucoma and other ophthalmic diseases. However, just as every physiologic fluid pressure fluctuates, cerebrospinal fluid pressure (CSFP) is similarly dynamic. Coupling this with the difficulty in measuring the pressure, there are many obstacles in furthering this field of study. This review highlights some of the difficulties in CSFP research, including fluid compartmentalization, estimation equations, and pressure fluctuation. Keeping these limitations in mind will hopefully improve the quality and context of this burgeoning field.

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“…We adopted an experimental approach introduced by our group to image with OCT the posterior pole of healthy monkeys pre-mortem and post-mortem while at several controlled IOP levels. 4,[36][37][38] We then analyzed the images to quantify acute IOP-induced LC deformations and identify any differences between pre-mortem and post-mortem responses.…”

Section: Introductionmentioning

confidence: 99%

Comparing acute IOP-induced lamina cribrosa deformations pre-mortem and post-mortem

Wei

Hua

Yang

et al. 2022

Preprint

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Purpose: Lamina cribrosa (LC) deformations caused by elevated intraocular pressure (IOP) are believed to contribute to glaucomatous neuropathy and have therefore been extensively studied, in many conditions from in-vivo to ex-vivo. We compare acute IOP-induced global and local LC deformations immediately before (pre-mortem) and after (post-mortem) sacrifice by exsanguination. Methods: The optic nerve heads of three healthy monkeys 12-15 years old were imaged with spectral-domain optical coherence tomography under controlled IOP pre-mortem and post-mortem. Volume scans were acquired at baseline IOP (8-10 mmHg) and at 15, 30, and 40 mmHg IOP. A digital volume correlation technique was used to determine the IOP-induced 3D LC deformations (strains) in regions visible pre-mortem and post-mortem. Results: Both conditions exhibited similar nonlinear relationships between IOP increases and LC deformations. Median effective and shear strains were, on average over all eyes and pressures, smaller post-mortem than pre-mortem, by 14% and 11%, respectively (P's < 0.001). Locally, however, the differences in LC deformation between conditions were variable. Some regions were subjected pre-mortem to triple the strains observed post-mortem, and others suffered smaller deformations pre-mortem than post-mortem. Conclusions: Increasing IOP acutely caused nonlinear LC deformations with an overall smaller effect post-mortem than pre-mortem. Locally, deformations pre-mortem and post-mortem were sometimes substantially different. We suggest that the differences may be due to weakened mechanical support from the unpressurized central retinal vessels post-mortem. Translational Relevance: Additional to the important pre-mortem information, comparison with post-mortem provides a unique context essential to understand the translational relevance of all post-mortem biomechanics literature.

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Interplay between intraocular and intracranial pressure effects on the optic nerve head in vivo

Cited by 13 publications

References 68 publications

Relative Contributions of Intraocular and Cerebrospinal Fluid Pressures to the Biomechanics of the Lamina Cribrosa and Laminar Neural Tissues

Relative Contributions of Intraocular and Cerebrospinal Fluid Pressures to the Biomechanics of the Lamina Cribrosa and Laminar Neural Tissues

Problems in CSF and Ophthalmic Disease Research

Comparing acute IOP-induced lamina cribrosa deformations pre-mortem and post-mortem

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