Research Papers

Intracranial Pressure Influences the Behavior of the Optic Nerve Head

[+] Author and Article Information
Yi Hua, Junfei Tong

Department of Mechanical and
Materials Engineering,
University of Nebraska-Lincoln,
Lincoln, NE 68588-0656

Deepta Ghate

Stanley Truhlsen Eye Institute,
University of Nebraska Medical Center,
Omaha, NE 68105-1119;
Center for Advanced Surgical Technology,
University of Nebraska Medical Center,
Omaha, NE 68198-6245

Sachin Kedar

Stanley Truhlsen Eye Institute,
University of Nebraska Medical Center,
Omaha, NE 68105-1119;
Department of Neurological Sciences,
University of Nebraska Medical Center,
Omaha, NE 68198-8440

Linxia Gu

Department of Mechanical and
Materials Engineering,
University of Nebraska-Lincoln,
Lincoln, NE 68588-0656;
Center for Advanced Surgical Technology,
University of Nebraska Medical Center,
Omaha, NE 68198-6245;
Nebraska Center for Materials and Nanoscience,
Lincoln, NE 68588-0656
e-mail: lgu2@unl.edu

1Y. Hua and J. Tong contributed equally to this work.

2Corresponding author.

Manuscript received March 26, 2016; final manuscript received November 20, 2016; published online January 23, 2017. Assoc. Editor: Thao (Vicky) Nguyen.

J Biomech Eng 139(3), 031003 (Jan 23, 2017) (6 pages) Paper No: BIO-16-1119; doi: 10.1115/1.4035406 History: Received March 26, 2016; Revised November 20, 2016

In this work, the biomechanical responses of the optic nerve head (ONH) to acute elevations in intracranial pressure (ICP) were systematically investigated through numerical modeling. An orthogonal experimental design was developed to quantify the influence of ten input factors that govern the anatomy and material properties of the ONH on the peak maximum principal strain (MPS) in the lamina cribrosa (LC) and postlaminar neural tissue (PLNT). Results showed that the sensitivity of ONH responses to various input factors was region-specific. In the LC, the peak MPS was most strongly dependent on the sclera thickness, LC modulus, and scleral canal size, whereas in the PLNT, the peak MPS was more sensitive to the scleral canal size, neural tissue modulus, and pia mater modulus. The enforcement of clinically relevant ICP in the retro-orbital subarachnoid space influenced the sensitivity analysis. It also induced much larger strains in the PLNT than in the LC. Moreover, acute elevation of ICP leads to dramatic strain distribution changes in the PLNT, but had minimal impact on the LC. This work could help to better understand patient-specific responses, to provide guidance on biomechanical factors resulting in optic nerve diseases, such as glaucoma, papilledema, and ischemic optic neuropathy, and to illuminate the possibilities for exploiting their potential to treat and prevent ONH diseases.

Copyright © 2017 by ASME
Your Session has timed out. Please sign back in to continue.


Quigley, H. A. , and Broman, A. T. , 2006, “ The Number of People With Glaucoma Worldwide in 2010 and 2020,” Br. J. Ophthalmol., 90(3), pp. 262–267. [CrossRef] [PubMed]
Hattar, S. , Liao, H.-W. , Takao, M. , Berson, D. M. , and Yau, K.-W. , 2002, “ Melanopsin-Containing Retinal Ganglion Cells: Architecture, Projections, and Intrinsic Photosensitivity,” Science, 295(5557), pp. 1065–1070. [CrossRef] [PubMed]
Morgan, W. H. , Yu, D.-Y. , Cooper, R. L. , Alder, V. A. , Cringle, S. J. , and Constable, I. J. , 1995, “ The Influence of Cerebrospinal Fluid Pressure on the Lamina Cribrosa Tissue Pressure Gradient,” Invest. Ophthalmol. Visual Sci., 36, pp. 1163–1172.
Morgan, W. H. , Yu, D.-Y. , Alder, V. A. , Cringle, S. J. , Cooper, R. L. , House, P. H. , and Constable, I. J. , 1998, “ The Correlation Between Cerebrospinal Fluid Pressure and Retrolaminar Tissue Pressure,” Invest. Ophthalmol. Visual Sci., 39, pp. 1419–1428.
Berdahl, J. P. , Allingham, R. R. , and Johnson, D. H. , 2008, “ Cerebrospinal Fluid Pressure Is Decreased in Primary Open-Angle Glaucoma,” Ophthalmology, 115(5), pp. 763–768. [CrossRef] [PubMed]
Taibbi, G. , Cromwell, R. L. , Kapoor, K. G. , Godley, B. F. , and Vizzeri, G. , 2013, “ The Effect of Microgravity on Ocular Structures and Visual Function: A Review,” Surv. Ophthalmol., 58(2), pp. 155–163. [CrossRef] [PubMed]
Pang, J.-J. , Frankfort, B. J. , Gross, R. L. , and Wu, S. M. , 2015, “ Elevated Intraocular Pressure Decreases Response Sensitivity of Inner Retinal Neurons in Experimental Glaucoma Mice,” Proc. Natl. Acad. Sci., 112(8), pp. 2593–2598. [CrossRef]
Yang, H. , Downs, J. C. , Sigal, I. A. , Roberts, M. D. , Thompson, H. , and Burgoyne, C. F. , 2009, “ Deformation of the Normal Monkey Optic Nerve Head Connective Tissue Following Acute IOP Elevation Within 3-D Histomorphometric Reconstructions,” Invest. Ophthalmol. Visual Sci., 50(12), pp. 5785–5799. [CrossRef]
Lee, D. S. , Lee, E. J. , Kim, T.-W. , Park, Y. H. , Kim, J. , Lee, J. W. , and Kim, S. , 2015, “ Influence of Translaminar Pressure Dynamics on the Position of the Anterior Lamina Cribrosa Surface Translaminar Pressure Dynamics and LC Position,” Invest. Ophthalmol. Visual Sci., 56(5), pp. 2833–2841. [CrossRef]
Feola, A. J. , Myers, J. G. , Raykin, J. , Mulugeta, L. , Nelson, E. S. , Samuels, B. C. , and Ethier, C. R. , 2016, “ Finite Element Modeling of Factors Influencing Optic Nerve Head Deformation Due to Intracranial Pressure ICP Affects ONH Deformation,” Invest. Ophthalmol. Visual Sci., 57(4), pp. 1901–1911. [CrossRef]
Fazio, M. A. , Grytz, R. , Morris, J. S. , Bruno, L. , Gardiner, S. K. , Girkin, C. A. , and Downs, J. C. , 2014, “ Age-Related Changes in Human Peripapillary Scleral Strain,” Biomech. Model Mechanobiol., 13(3), pp. 551–563. [CrossRef] [PubMed]
Burgoyne, C. F. , Downs, J. C. , Bellezza, A. J. , Suh, J.-K. F. , and Hart, R. T. , 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. Retinal Eye Res., 24(1), pp. 39–73. [CrossRef]
Mi, X.-S. , Yuan, T.-F. , and So, K.-F. , 2014, “ The Current Research Status of Normal Tension Glaucoma,” Clin. Interventions Aging, 2014(9), pp. 1563–1571.
Ren, R. , Wang, N. , Zhang, X. , Tian, G. , and Jonas, J. B. , 2012, “ Cerebrospinal Fluid Pressure Correlated With Body Mass Index,” Graefe's Arch. Clin. Exp. Ophthalmol., 250(3), pp. 445–446. [CrossRef]
Sigal, I. A. , Flanagan, J. G. , Tertinegg, I. , and Ethier, C. R. , 2004, “ Finite Element Modeling of Optic Nerve Head Biomechanics,” Invest. Ophthalmol. Visual Sci., 45(12), pp. 4378–4387. [CrossRef]
Siaudvytyte, L. , Januleviciene, I. , Ragauskas, A. , Bartusis, L. , Siesky, B. , and Harris, A. , 2015, “ Update in Intracranial Pressure Evaluation Methods and Translaminar Pressure Gradient Role in Glaucoma,” Acta Ophthalmol., 93(1), pp. 9–15. [CrossRef] [PubMed]
Killer, H. , Laeng, H. , Flammer, J. , and Groscurth, P. , 2003, “ Architecture of Arachnoid Trabeculae, Pillars, and Septa in the Subarachnoid Space of the Human Optic Nerve: Anatomy and Clinical Considerations,” Br. J. Ophthalmol., 87(6), pp. 777–781. [CrossRef] [PubMed]
Balaratnasingam, C. , Morgan, W. H. , Johnstone, V. , Pandav, S. S. , Cringle, S. J. , and Yu, D.-Y. , 2009, “ Histomorphometric Measurements in Human and Dog Optic Nerve and an Estimation of Optic Nerve Pressure Gradients in Human,” Exp. Eye Res., 89(5), pp. 618–628. [CrossRef] [PubMed]
Reina, M. A. , Casasola, O. D. L. , López, A. , De Andrés, J. A. , Mora, M. , and Fernández, A. , 2002, “ The Origin of the Spinal Subdural Space: Ultrastructure Findings,” Anesth. Analg., 94(4), pp. 991–995. [CrossRef] [PubMed]
Barraglioli, J. , and Kamm, R. , 1984, “ Measurements of the Compressive Properties of Scleral Tissue,” Invest. Ophthalmol. Visual Sci., 25, pp. 59–65. http://iovs.arvojournals.org/article.aspx?articleid=2159718
Woo, S.-Y. , Kobayashi, A. , Schlegel, W. , and Lawrence, C. , 1972, “ Nonlinear Material Properties of Intact Cornea and Sclera,” Exp. Eye Res., 14(1), pp. 29–39. [CrossRef] [PubMed]
Jones, I. , Warner, M. , and Stevens, J. , 1992, “ Mathematical Modelling of the Elastic Properties of Retina: A Determination of Young's Modulus,” Eye, 6(6), pp. 556–559. [CrossRef] [PubMed]
Ozawa, H. , Matsumoto, T. , Ohashi, T. , Sato, M. , and Kokubun, S. , 2004, “ Mechanical Properties and Function of the Spinal Pia Mater,” J. Neurosurg. Spine, 1(1), pp. 122–127. [CrossRef] [PubMed]
Chafi, M. , Karami, G. , and Ziejewski, M. , 2010, “ Biomechanical Assessment of Brain Dynamic Responses Due to Blast Pressure Waves,” Ann. Biomed. Eng., 38(2), pp. 490–504. [CrossRef] [PubMed]
Kleiven, S. , 2007, “ Predictors for Traumatic Brain Injuries Evaluated Through Accident Reconstructions,” Stapp Car Crash J., 51, pp. 81–114. [PubMed]
Goetz, C. G. , 2007, Textbook of Clinical Neurology, Elsevier Health Sciences, Atlanta, GA.
Berdahl, J. P. , Fautsch, M. P. , Stinnett, S. S. , and Allingham, R. R. , 2008, “ Intracranial Pressure in Primary Open Angle Glaucoma, Normal Tension Glaucoma, and Ocular Hypertension: A Case-Control Study,” Invest. Ophthalmol Visual Sci., 49(12), pp. 5412–5418. [CrossRef]
Perry, R. B. , and Rose, J. C. , 1958, “ The Clinical Measurement of Retinal Arterial Pressure,” Circulation, 18(5), pp. 864–870. [CrossRef] [PubMed]
Taguchi, G. , 1986, Introduction to Quality Engineering: Designing Quality Into Products and Processes, Quality Resources, Tokyo, Japan.
Taguchi, G. , and Taguchi, G. , 1987, System of Experimental Design; Engineering Methods to Optimize Quality and Minimize Costs, UNIPUB/Kraus International Publications, White Plains, NY.
Dey, A. , 1985, Orthogonal Fractional Factorial Designs, Wiley, New York.
Sigal, I. A. , Flanagan, J. G. , and Ethier, C. R. , 2005, “ Factors Influencing Optic Nerve Head Biomechanics,” Invest. Ophthalmol. Visual Sci., 46(11), pp. 4189–4199. [CrossRef]
Roy, R. K. , 2010, A Primer on the Taguchi Method, Society of Manufacturing Engineers, Dearborn, MI.
Keppel, G. , 1991, Design and Analysis: A Researcher's Handbook, Prentice-Hall, Englewood Cliffs, NJ.
Mao, H. , Zhang, L. , Yang, K. H. , and King, A. I. , 2006, “ Application of a Finite Element Model of the Brain to Study Traumatic Brain Injury Mechanisms in the Rat,” Stapp Car Crash J., 50, pp. 583–600. [PubMed]
Coudrillier, B. , Boote, C. , Quigley, H. A. , and Nguyen, T. D. , 2013, “ Scleral Anisotropy and Its Effects on the Mechanical Response of the Optic Nerve Head,” Biomech. Model Mechanabiol., 12(5), pp. 941–963. [CrossRef]
Downs, J. C. , Suh, J. , Thomas, K. A. , Bellezza, A. J. , Hart, R. T. , and Burgoyne, C. F. , 2005, “ Viscoelastic Material Properties of the Peripapillary Sclera in Normal and Early-Glaucoma Monkey Eyes,” Invest. Ophthalmol. Visual Sci., 46(2), pp. 540–546. [CrossRef]
Grytz, R. , Sigal, I. A. , Ruberti, J. W. , Meschke, G. , and Downs, J. C. , 2012, “ Lamina Cribrosa Thickening in Early Glaucoma Predicted by a Microstructure Motivated Growth and Remodeling Approach,” Mech. Mater., 44, pp. 99–109. [CrossRef] [PubMed]
Kim, T.-W. , Kagemann, L. , Girard, M. J. , Strouthidis, N. G. , Sung, K. R. , Leung, C. K. , Schuman, J. S. , and Wollstein, G. , 2013, “ Imaging of the Lamina Cribrosa in Glaucoma: Perspectives of Pathogenesis and Clinical Applications,” Current Eye Res., 38(9), pp. 903–909. [CrossRef]
Hernandez, M. R. , 2000, “ The Optic Nerve Head in Glaucoma: Role of Astrocytes in Tissue Remodeling,” Prog. Retinal Eye Res., 19(3), pp. 297–321. [CrossRef]


Grahic Jump Location
Fig. 1

Model geometry. Left: full view of the model with axis of symmetry and equator. Right: Zoom-in view of the optic nerve head region.

Grahic Jump Location
Fig. 2

Pareto chart of peak maximum principal strain (MPS) in lamina cribrosa (LC) and postlaminar neural tissue (PLNT) to various input factors. A—scleral canal size (mm), B—sclera thickness (mm), C—lamina cribrosa thickness (mm), D—pia mater thickness (mm), E—dura mater thickness (mm), F—sclera modulus (MPa), G—lamina cribrosa modulus (MPa), H—neural tissue modulus (MPa), I—pia mater modulus (MPa), and J—dura mater modulus (MPa).

Grahic Jump Location
Fig. 3

Distributions of maximum principal strain in the lamina cribrosa and postlaminar neural tissue to the most sensitive input factors

Grahic Jump Location
Fig. 4

Displacement of the pia mater at different intracranial pressures (ICPs)



Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In