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Finite element analysis of trans-lamina cribrosa pressure difference on optic nerve head biomechanics: the Beijing Intracranial and Intraocular Pressure Study

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Abstract

The present study aims to assess the potential difference of biomechanical response of the optic nerve head to the same level of trans-lamina cribrosa pressure difference (TLCPD) induced by a reduced cerebrospinal fluid pressure (CSFP) or an elevated intraocular pressure (IOP). A finite element model of optic nerve head tissue (pre- and post-laminar neural tissue, lamina cribrosa, sclera, and pia mater) was constructed. Computed stresses, deformations, and strains were compared at each TLCPD step caused by reduced CSFP or elevated IOP. The results showed that elevating TLCPD increased the strain in optic nerve head, with the largest strains occurring in the neural tissue around the sclera ring. Relative to a baseline TLCPD of 10 mmHg, at a same TLCPD of 18 mmHg, the pre-laminar neural tissue experienced 11.10% first principal strain by reduced CSFP and 13.66% by elevated IOP, respectively. The corresponding values for lamina cribrosa were 6.09% and 6.91%. In conclusion, TLCPD has a significant biomechanical impact on optic nerve head tissue and, more prominently, within the pre-laminar neural tissue and lamina cribrosa. Comparatively, reducing CSFP showed smaller strain than elevating IOP even at a same level of TLCPD on ONH tissue, indicating a different potential role of low CSFP in the pathogenesis of glaucoma.

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References

  • Band, L.R., Hall, C.L., Richardson, G., Jensen, O.E., Siggers, J.H., and Foss, A.J.E. (2009). Intracellular flow in optic nerve axons: A mechanism for cell death in glaucoma. Invest Ophthalmol Vis Sci 50, 3750–3758.

    Article  Google Scholar 

  • Beckel, J.M., Argall, A.J., Lim, J.C., Xia, J., Lu, W., Coffey, E.E., Macarak, E.J., Shahidullah, M., Delamere, N.A., Zode, G.S., et al. (2014). Mechanosensitive release of adenosine 5’-triphosphate through pannexin channels and mechanosensitive upregulation of pannexin channels in optic nerve head astrocytes: A mechanism for purinergic involvement in chronic strain. Glia 62, 1486–1501.

    Article  Google Scholar 

  • Berdahl, J.P., Allingham, R.R., and Johnson, D.H. (2008). Cerebrospinal fluid pressure is decreased in primary open-angle glaucoma. Ophthalmology 115, 763–768.

    Article  Google Scholar 

  • Downs, J.C., Suh, J.K.F., Thomas, K.A., Bellezza, A.J., Burgoyne, C.F., and Hart, R.T. (2003). Viscoelastic characterization of peripapillary sclera: Material properties by quadrant in rabbit and monkey eyes. J Biomech Eng 125, 124–131.

    Article  Google Scholar 

  • Edwards, M.E., and Good, T.A. (2001). Use of a mathematical model to estimate stress and strain during elevated pressure induced lamina cribrosa deformation. Curr Eye Res 23, 215–225.

    Article  CAS  Google Scholar 

  • Feola, A., Abramowitch, S., Jallah, Z., Stein, S., Barone, W., Palcsey, S., and Moalli, P. (2013). Deterioration in biomechanical properties of the vagina following implantation of a high-stiffness prolapse mesh. BJOG, 120, 224–232.

    Article  CAS  Google Scholar 

  • Geijssen, H.C. (1991). Studies on Normal Pressure Glaucoma. Amsterdam: Kugler Publication.

    Google Scholar 

  • Jonas, J.B., Gusek, G.C., Guggenmoos-Holzmann, I., and Naumann, G.O. H. (1988). Size of the optic nerve scleral canal and comparison with intravital determination of optic disc dimensions. Graefe’s Arch Clin Exp Ophthalmol 226, 213–215.

    Article  CAS  Google Scholar 

  • Jonas, J.B., and Budde, W.M. (2000). Diagnosis and pathogenesis of glaucomatous optic neuropathy: Morphological aspects. Prog Retinal Eye Res 19, 1–40.

    Article  CAS  Google Scholar 

  • Jonas, J.B., Budde, W.M., Németh, J., Gründler, A.E., Mistlberger, A., and Hayler, J.K. (2001). Central retinal vessel trunk exit and location of glaucomatous parapapillary atrophy in glaucoma. Ophthalmology 108, 1059–1064.

    Article  CAS  Google Scholar 

  • Jonas, J.B., Berenshtein, E., and Holbach, L. (2003). Anatomic relationship between lamina cribrosa, intraocular space, and cerebrospinal fluid space. Invest Ophthalmol Vis Sci 44, 5189–5195.

    Article  Google Scholar 

  • Kozobolis, V., Konstantinidis, A., and Labiris, G. (2013). Recognizing a glaucomatous optic disc. In: Rumelt, S., ed. Glaucoma-Basic and Clinical Aspects. 749–750.

    Google Scholar 

  • Levy, N.S., Crapps, E.E., and Bonney, R.C. (1981). Displacement of the optic nerve head. Arch Ophthalmol 99, 2166–2174.

    Article  CAS  Google Scholar 

  • Liu, L., Li, X., Killer, H.E., Cao, K., Li, J., and Wang, N. (2019). Changes in retinal and choroidal morphology after cerebrospinal fluid pressure reduction: A Beijing iCOP study. Sci China Life Sci 62, 268–271.

    Article  CAS  Google Scholar 

  • Morgan, W.H., Chauhan, B.C., Yu, D.Y., Cringle, S.J., Alder, V.A., and House, P.H. (2002). Optic disc movement with variations in intraocular and cerebrospinal fluid pressure. Invest Ophthalmol Vis Sci 43, 3236–3242.

    PubMed  Google Scholar 

  • Morgan, W.H., Yu, D.Y., and Balaratnasingam, C. (2008). The role of cerebrospinal fluid pressure in glaucoma pathophysiology: The dark side of the optic disc. J Glaucoma 17, 408–413.

    Article  Google Scholar 

  • Majima, T., Yasuda, K., Tsuchida, T., Tanaka, K., Miyakawa, K., Minami, A., and Hayashi, K. (2003). Stress shielding of patellar tendon: Effect on small-diameter collagenfibrils in a rabbit modele criterion for diffuse axonal injury in man. J Biomech 25, 917–923.

    Google Scholar 

  • Nagels, J., Stokdijk, M., and Rozing, P.M. (2003). Stress shielding and bone resorption in shoulder arthroplasty. J Shoulder Elbow Surg 12, 35–39.

    Article  Google Scholar 

  • Norman, R.E., Flanagan, J.G., Sigal, I.A., Rausch, S.M.K., Tertinegg, I., and Ethier, C.R. (2011). Finite element modeling of the human sclera: Influence on optic nerve head biomechanics and connections with glaucoma. Exp Eye Res 93, 4–12.

    Article  CAS  Google Scholar 

  • Olsen, T.W., Aaberg, S.Y., Geroski, D.H., and Edelhauser, H.F. (1998). Human sclera: Thickness and surface area. Am J Ophthalmol 125, 237–241.

    Article  CAS  Google Scholar 

  • Quigley, H.A., Addicks, E.M., and Green, W.R. (1982). Optic nerve damage in human glaucoma. Arch Ophthalmol 100, 135.

    Article  CAS  Google Scholar 

  • Quigley, H.A., Brown, A., and Dorman-Pease, M.E. (1991). Alterations in elastin of the optic nerve head in human and experimental glaucoma. British J Ophthalmol 75, 552–557.

    Article  CAS  Google Scholar 

  • Ren, R., Wang, N., Zhang, X., Cui, T., and Jonas, J.B. (2011). Trans-lamina cribrosa pressure difference correlated with neuroretinal rim area in glaucoma. Graefes Arch Clin Exp Ophthalmol 249, 1057–1063.

    Article  Google Scholar 

  • Roberts, M.D., Liang, Y., Sigal, I.A., Grimm, J., Reynaud, J., Bellezza, A., Burgoyne, C.F., and Downs, J.C. (2010). Correlation between local stress and strain and lamina cribrosa connective tissue volume fraction in normal monkey eyes. Invest Ophthalmol Vis Sci 51, 295–307.

    Article  Google Scholar 

  • Sigal, I.A., Flanagan, J.G., Tertinegg, I., and Ethier, C.R. (2004). Finite element modeling of optic nerve head biomechanics. Invest Ophthalmol Vis Sci 45, 4378–4387.

    Article  Google Scholar 

  • Sigal, I.A. (2011). An applet to estimate the IOP-induced stress and strain within the optic nerve head. Invest Ophthalmol Vis Sci 52, 5497–5506.

    Article  Google Scholar 

  • Triyoso, D.H., and Good, T.A. (1999). Pulsatile shear stress leads to dna fragmentation in human SH-SY5Y neuroblastoma cell line. J Physiol 515, 355–365.

    Article  CAS  Google Scholar 

  • Wang, N., Xie, X., Yang, D., Xian, J., Li, Y., Ren, R., Peng, X., Jonas, J.B., and Weinreb, R.N. (2012). Orbital cerebrospinal fluid space in glaucoma: The Beijing intracranial and intraocular pressure (iCOP) study. Ophthalmology 119, 2065–2073.e1.

    Article  Google Scholar 

  • Yang, D., Fu, J., Hou, R., Liu, K., Jonas, J.B., Wang, H., Chen, W., Li, Z., Sang, J., Zhang, Z., et al. (2014). Optic neuropathy induced by experimentally reduced cerebrospinal fluid pressure in monkeys. Invest Ophthalmol Vis Sci 55, 3067–3073.

    Article  Google Scholar 

  • Yang, H., Downs, J.C., Bellezza, A., Thompson, H., and Burgoyne, C.F. (2007). 3-D histomorphometry of the normal and early glaucomatous monkey optic nerve head: Prelaminar neural tissues and cupping. Invest Ophthalmol Vis Sci 48, 5068–5084.

    Article  Google Scholar 

  • Zhang, Z., Liu, D., Jonas, J.B., Wu, S., Kwong, J.M.K., Zhang, J., Liu, Q., Li, L., Lu, Q., Yang, D., et al. (2015). Axonal transport in the rat optic nerve following short-term reduction in cerebrospinal fluid pressure or elevation in intraocular pressure. Invest Ophthalmol Vis Sci 56, 4257–4266.

    Article  Google Scholar 

  • Zhivoderov, N.N., Zavalishin, N.N., and Neniukov, A.K. (1983). Mechanical properties of the dura mater of the human brain. Sudebnomeditsinsk Ekspert 26, 36–37.

    CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (81271005, 81300767), the Beijing Natural Science Foundation (7122038, 7162037), and the Basic-Clinical Research Cooperation Funding of Capital Medical University (2016-JLPT-Y03). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Correspondence to Ningli Wang.

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Mao, Y., Yang, D., Li, J. et al. Finite element analysis of trans-lamina cribrosa pressure difference on optic nerve head biomechanics: the Beijing Intracranial and Intraocular Pressure Study. Sci. China Life Sci. 63, 1887–1894 (2020). https://doi.org/10.1007/s11427-018-1585-8

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