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Optic nerve head damage relation to intracranial pressure and corneal properties of eye in glaucoma risk assessment

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Abstract

This work presents results from numerical simulations of optic nerve head’s (ONH) biomechanical behavior during exposure to elevated intraocular (IOP) and/or intracranial pressure (ICP) for ocular hypertension conditions. At the same time, a range of geometric and material properties of the eye structure and their interrelation with elevated IOP and ICP values are investigated. These simulations are performed on a generic model of the eye, which allows parametrical modification of geometric and material properties. Our main interest is in measuring ONH’s potential damage in ocular hypertension due to intracranial pressure. Simulation results indicate a significant role of ICP in post-laminar neural tissue failure and a possible role of central corneal thickness (CCT) and scleral modulus in clinical assessment and treatment of patients with ocular hypertension (OHT). Specifically, CCT was found to affect ONH at early stages of damage in ocular hypertension conditions, and high scleral modulus seems to result in reduced shear failure in lamina cribrosa in a similar OHT state. These findings suggest that CCT could be a risk factor for glaucoma in OHT patients at initial stage along with cornea stiffness.

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References

  1. Quigley H, Broman AT (2006) The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol 90(3):262–267

    Article  CAS  Google Scholar 

  2. Sigal IA, Flanagan JG, Tertinegg I, Ethier CR (2009) Modeling individual-specific human optic nerve head biomechanics. Part II: influence of material properties. Biomech Model Mechanobiol 8(2):99–109. https://doi.org/10.1007/s10237-008-0119-0

    Article  PubMed  Google Scholar 

  3. Hattar S, Liao HW, Takao M, Berson DM, Yau KW (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science. 295(5557):1065–1070. https://doi.org/10.1126/science.1069609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Sigal IA, Ethier CR (2009) Biomechanics of the optic nerve head. Exp Eye Res 88(4):799–807

    Article  CAS  Google Scholar 

  5. Yan DB, Coloma FM, Metheetrairut A, Trope GE, Heathcote JG, Ethier CR (1994) Deformation of the lamina cribrosa by elevated intraocular pressure. Br J Ophthalmol 78(8):643–648. https://doi.org/10.1136/bjo.78.8.643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hernandez MR (2000) The optic nerve head in glaucoma: role of astrocytes in tissue remodeling. Prog Retin Eye Res 19(3):297–321

    Article  CAS  Google Scholar 

  7. Hiraoka M, Inoue K, Ninomiya T, Takada M (2012) Ischaemia in the Zinn-Haller circle and glaucomatous optic neuropathy in macaque monkeys. Br J Ophthalmol 96(4):597–603. https://doi.org/10.1136/bjophthalmol-2011-300831

    Article  PubMed  PubMed Central  Google Scholar 

  8. Burgoyne CF, Crawford Downs J, Bellezza AJ, Francis Suh JK, Hart RT (2005) The optic nerve head as a biomechanical structure: a new paradigm for understanding the role of IOP-related stress and strain in the pathophysiology of glaucomatous optic nerve head damage. Prog Retin Eye Res 24(1):39–73

    Article  Google Scholar 

  9. Xie X, Chen W, Li Z, Thomas R, Li Y, Xian J, Yang D, Wang H, Zhang S, Kang Z, Wang N, the Beijing Intraocular and Intracranial Study Group (2018) Noninvasive evaluation of cerebrospinal fluid pressure in ocular hypertension: a preliminary study. Acta Ophthalmol 96(5):e570–e576. https://doi.org/10.1111/aos.13724

    Article  PubMed  Google Scholar 

  10. Berdahl JP, Fautsch MP, Stinnett SS, Allingham RR (2008) Intracranial pressure in primary open angle glaucoma, normal tension glaucoma, and ocular hypertension: a case-control study. Invest Ophthalmol Vis Sci 49(12):5412–5418. https://doi.org/10.1167/iovs.08-2228

    Article  PubMed  PubMed Central  Google Scholar 

  11. Ren R, Zhang X, Wang N, Li B, Tian G, Jonas JB (2011) Cerebrospinal fluid pressure in ocular hypertension. Acta Ophthalmol 89(2):e142–e148. https://doi.org/10.1111/j.1755-3768.2010.02015.x

    Article  PubMed  Google Scholar 

  12. Johnson CS, Mian SI, Moroi S, Epstein D, Izatt J, Afshari NA (2007) Role of corneal elasticity in damping of intraocular pressure. Investig Ophthalmol Vis Sci 48(6):2540–2544. https://doi.org/10.1167/iovs.06-0719

    Article  Google Scholar 

  13. Sigal IA, Flanagan JG, Ethier CR (2005) Factors influencing optic nerve head biomechanics. Investig Ophthalmol Vis Sci 46(11):4189–4199. https://doi.org/10.1167/iovs.05-0541

    Article  Google Scholar 

  14. Gordon MO, Beiser JA, Brandt JD et al (2002) The ocular hypertension treatment study: baseline factors that predict the onset of primary open-angle glaucoma. Arch Ophthalmol 120(6):714–720. https://doi.org/10.1001/archopht.120.6.714

    Article  PubMed  Google Scholar 

  15. Herndon LW, Weizer JS, Stinnett SS (2004) Central corneal thickness as a risk factor for advanced glaucoma damage. Arch Ophthalmol 122(1):17–21

    Article  Google Scholar 

  16. Lam CK, Sundaraj K, Nazri Sulaiman M (2012) Virtual simulation of eyeball and extraocular muscle reaction during cataract surgery. Procedia Engineering 41:150–155

    Article  Google Scholar 

  17. Tse KM, Lee HP, Shabana N, Loon SC, Watson PG, Thean SYLH (2012) Do shapes and dimensions of scleral flap and sclerostomy influence aqueous outflow in trabeculectomy? A finite element simulation approach. Br J Ophthalmol 96(3):432–437. https://doi.org/10.1136/bjophthalmol-2011-300228

    Article  PubMed  Google Scholar 

  18. Lam CK, Sundaraj K, Sulaiman MN (2013) Virtual reality simulator for phacoemulsification cataract surgery education and training. Procedia Computer Science 18:742–748

    Article  Google Scholar 

  19. Feola AJ, Myers JG, Raykin J, Mulugeta L, Nelson ES, Samuels BC, Ethier CR (2016) Finite element modeling of factors influencing optic nerve head deformation due to intracranial pressure. Invest Opthalmol Vis Sci 57(4):1901–1911. https://doi.org/10.1167/iovs.15-17573

    Article  Google Scholar 

  20. Hua Y, Tong J, Ghate D, Kedar S, Gu L (2017) Intracranial pressure influences the behavior of the optic nerve head. J Biomech Eng 139(3):031003. https://doi.org/10.1115/1.4035406

    Article  Google Scholar 

  21. I a S, Flanagan JG, Tertinegg I, Ethier CR (2004) Finite element modeling of optic nerve head biomechanics. Invest Ophthalmol Vis Sci 45(12):4378–4387. https://doi.org/10.1167/iovs.04-0133

    Article  Google Scholar 

  22. Ren R, Wang N, Zhang X, Tian G, Jonas JB (2012) Cerebrospinal fluid pressure correlated with body mass index. Graefes Arch Clin Exp Ophthalmol 250(3):445–446. https://doi.org/10.1007/s00417-011-1746-1

    Article  PubMed  Google Scholar 

  23. Taguchi G (1986) Introduction to quality engineering: designing quality into products and processes. In: A productivity organization (No. 658.562 T3)

    Google Scholar 

  24. Hua Y, Voorhees AP, Sigal IA (2018) Cerebrospinal fluid pressure: revisiting factors influencing optic nerve head biomechanics. Invest Ophthalmol Vis Sci 59(1):154–165. https://doi.org/10.1167/iovs.17-22488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Leung LKK, Ko MWL, Lam DCC (2012) Effect of age-stiffening tissues and intraocular pressure on optic nerve damages. Mol Cell Biomech 9(2):157–173

    PubMed  Google Scholar 

  26. Vurgese S, Panda-Jonas S, Jonas JB (2012) Scleral thickness in human eyes. PLoS One 7(1):e29692. https://doi.org/10.1371/journal.pone.0029692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shimmyo M, Ross AJ, Moy A, Mostafavi R (2003) Intraocular pressure, Goldmann applanation tension, corneal thickness, and corneal curvature in Caucasians, Asians, Hispanics, and African Americans. Am J Ophthalmol 136(4):603–613. https://doi.org/10.1016/S0002-9394(03)00424-0

    Article  PubMed  Google Scholar 

  28. Ren R, Wang N, Li B, Li L, Gao F, Xu X, Jonas JB (2009) Lamina cribrosa and peripapillary sclera histomorphometry in normal and advanced glaucomatous chinese eyes with various axial length. Investig Ophthalmol Vis Sci 50(5):2175–2184. https://doi.org/10.1167/iovs.07-1429

    Article  Google Scholar 

  29. Sing NM, Anderson SF, Townsend JC (2000) The normal optic nerve head. Optom Vis Sci 77(6):293–301

    Article  CAS  Google Scholar 

  30. Hamilton KE, Pye DC (2008) Young’s modulus in normal corneas and the effect on applanation tonometry. Optom Vis Sci 85(6):445–450. https://doi.org/10.1097/OPX.0b013e3181783a70

    Article  PubMed  Google Scholar 

  31. B a T, Thacker JG (1994) Three-dimensional computer model of the human buttocks, in vivo. J Rehabil Res Dev 31:111–111

    Google Scholar 

  32. Power E, Stitzel J, West R, Herring I (2001) A non linear finite element model of the human eye for large deformation loading. Proc. 25th … (pp. 44–45)

  33. Beisheim JR, Sinclair GB (2003) On the three-dimensional finite element analysis of dovetail attachments. J Turbomach 125(2):372–379. https://doi.org/10.1115/1.1539867

    Article  Google Scholar 

  34. Weller RO (2005) Microscopic morphology and histology of the human meninges. Morphologie. 89(284):22–34

    Article  CAS  Google Scholar 

  35. Allingham RR, Damji K, Freedman S et al (2011) Shields textbook of glaucoma, 6th edn

    Google Scholar 

  36. Woo SLY, Kobayashi AS, Schlegel WA, Lawrence C (1972) Nonlinear material properties of intact cornea and sclera. Exp Eye Res 14(1):29–39. https://doi.org/10.1016/0014-4835(72)90139-X

    Article  CAS  PubMed  Google Scholar 

  37. McEwan W, Belavendram N, Abou-Ali M (1992) Taguchi methods and expert systems in fabrication design. Int J Press Vessel Pip 53(1):47–61. https://doi.org/10.1016/0308-0161(93)90103-Z

    Article  Google Scholar 

  38. Edwards ME, Wang SSS, Good TA (2001) Role of viscoelastic properties of differentiated SH-SY5Y human neuroblastoma cells in cyclic shear stress injury. Biotechnol Prog 17(4):760–767. https://doi.org/10.1021/bp010040m

    Article  CAS  PubMed  Google Scholar 

  39. Grytz R, Meschke G, Jonas JB (2011) The collagen fibril architecture in the lamina cribrosa and peripapillary sclera predicted by a computational remodeling approach. Biomech Model Mechanobiol 10(3):371–382. https://doi.org/10.1007/s10237-010-0240-8

    Article  PubMed  Google Scholar 

  40. Grytz R, Sigal IA, Ruberti JW, Meschke G, Crawford Downs J (2012) Lamina cribrosa thickening in early glaucoma predicted by a microstructure motivated growth and remodeling approach. Mech Mater 44:99–109. https://doi.org/10.1016/j.mechmat.2011.07.004

    Article  PubMed  PubMed Central  Google Scholar 

  41. Ionescu I, Guilkey JE, Berzins M, Kirby RM, Weiss JA (2006) Simulation of soft tissue failure using the material point method. J Biomech Eng 128(6):917–924. https://doi.org/10.1115/1.2372490

    Article  PubMed  Google Scholar 

  42. Caselli RJ, Boeve BF (2007) Textbook of clinical neurology

    Google Scholar 

  43. Perry RB, Rose JC (1958) The clinical measurement of retinal arterial pressure. Circulation. 18(5):864–870. https://doi.org/10.1161/01.CIR.18.5.864

    Article  CAS  PubMed  Google Scholar 

  44. Kiening KL, Schoening W, Unterberg AW et al (2005) Assessment of the relationship between age and continuous intracranial compliance. In: Acta Neurochirurgica, Supplementum, pp 293–297

    Google Scholar 

  45. Albon J, Purslow PP, Karwatowski WSS, Easty DL (2000) Age related compliance of the lamina cribrosa in human eyes. Br J Ophthalmol 84(3):318–323. https://doi.org/10.1136/bjo.84.3.318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ren R, Jonas JB, Tian G, Zhen Y, Ma K, Li S, Wang H, Li B, Zhang X, Wang N (2010) Cerebrospinal fluid pressure in glaucoma. A prospective study. Ophthalmology. 117(2):259–266. https://doi.org/10.1016/j.ophtha.2009.06.058

    Article  PubMed  Google Scholar 

  47. Thornton IL, Dupps WJ, Roy AS, Krueger RR (2009) Biomechanical effects of intraocular pressure elevation on optic nerve/lamina cribrosa before and after peripapillary scleral collagen cross-linking. Investig Ophthalmol Vis Sci 50(3):1227–1233. https://doi.org/10.1167/iovs.08-1960

    Article  Google Scholar 

  48. Norman RE, Flanagan JG, Rausch SMK, Sigal IA, Tertinegg I, Eilaghi A, Portnoy S, Sled JG, Ethier CR (2010) Dimensions of the human sclera: thickness measurement and regional changes with axial length. Exp Eye Res 90(2):277–284. https://doi.org/10.1016/j.exer.2009.11.001

    Article  CAS  PubMed  Google Scholar 

  49. Berdahl JP, Allingham RR, Johnson DH (2008) Cerebrospinal fluid pressure is decreased in primary open-angle glaucoma. Ophthalmology. 115(5):763–768. https://doi.org/10.1016/j.ophtha.2008.01.013

    Article  PubMed  Google Scholar 

  50. Jonas JB, Ritch R, Panda-Jonas S (2015) Cerebrospinal fluid pressure in the pathogenesis of glaucoma. In: Progress in brain research, vol 46, pp 67–83

    Google Scholar 

  51. Brandt JD, Beiser JA, Kass MA, Gordon MO (2001) Central corneal thickness in the ocular hypertension treatment study (OHTS). Ophthalmology. 108(10):1779–1788. https://doi.org/10.1016/S0161-6420(01)00760-6

    Article  CAS  PubMed  Google Scholar 

  52. Johnson M, Kass MA, Moses RA, Grodzki WJ (1978) Increased corneal thickness simulating elevated intraocular pressure. Arch Ophthalmol 96(4):664–665. https://doi.org/10.1001/archopht.1978.03910050360012

    Article  CAS  PubMed  Google Scholar 

  53. Whitacre MM, Stein RA, Hassanein K (1993) The effect of corneal thickness on applanation tonometry. Am J Ophthalmol 115(5):592–596. https://doi.org/10.1016/S0002-9394(14)71455-2

    Article  CAS  PubMed  Google Scholar 

  54. Argus WA (1995) Ocular hypertension and central corneal thickness. Ophthalmology. 102(12):1810–1812. https://doi.org/10.1016/S0161-6420(95)30790-7

    Article  CAS  PubMed  Google Scholar 

  55. Hon Y, Chen GZ, Lu SH, Lam DCC, Lam AKC (2017) In vivo measurement of regional corneal tangent modulus. Sci Rep 7(1):14974. https://doi.org/10.1038/s41598-017-14750-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Soergel F, Muecke S, Pechhold W (2011) Corneal viscoelasticity spectra as a result of dynamic mechanical analysis. In: Advances in corneal research, pp 257–272

    Google Scholar 

  57. Zhang J, Wang L, Tian L et al (2019) Corneal biomechanical properties characterization using air-jet indentation based optical coherence tomography system (AIOCT). MATEC Web Conf 256. https://doi.org/10.1051/matecconf/201925601004

  58. Alonso-Caneiro D, Kowalczyk A, Wojtkowski M et al (2011) Assessment of corneal dynamics with high-speed swept source optical coherence tomography combined with an air puff system. Opt Express 19(15):14188–14199. https://doi.org/10.1364/oe.19.014188

    Article  CAS  PubMed  Google Scholar 

  59. Hollman KW, Shtein RM, Tripathy S, Kim K (2013) Using an ultrasound elasticity microscope to map three-dimensional strain in a porcine cornea. Ultrasound Med Biol 39(8):1451–1459. https://doi.org/10.1016/j.ultrasmedbio.2013.02.465

    Article  PubMed  PubMed Central  Google Scholar 

  60. Ramm L, Pillunat LE, Herber R et al (2019) Measurement of corneal biomechanical properties in diabetes mellitus using the ocular response analyzer and the Corvis ST. Cornea. 38:595–599. https://doi.org/10.1097/ico.0000000000001879

    Article  PubMed  Google Scholar 

  61. Girard MJA, Downs JC, Bottlang M et al (2009) Peripapillary and posterior scleral mechanics—part II: experimental and inverse finite element characterization. J Biomech Eng 131(5):051012. https://doi.org/10.1115/1.3113683

    Article  PubMed  PubMed Central  Google Scholar 

  62. Karimi A, Razaghi R, Navidbakhsh M, Sera T, Kudo S (2017) Mechanical properties of the human sclera under various strain rates: elastic, hyperelastic, and viscoelastic models. J Biomater Tissue Eng 7(8):686–695. https://doi.org/10.1166/jbt.2017.1609

    Article  Google Scholar 

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This work is partially supported by the Nazarbayev University individual grants 481-2018 and 445-2019.

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Correspondence to Chingis Kharmyssov.

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Kharmyssov, C., Abdildin, Y.G. & Kostas, K.V. Optic nerve head damage relation to intracranial pressure and corneal properties of eye in glaucoma risk assessment. Med Biol Eng Comput 57, 1591–1603 (2019). https://doi.org/10.1007/s11517-019-01983-2

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