Glaucomatous cupping of the lamina cribrosa: A review of the evidence for active progressive remodeling as a mechanism

Experimental Eye Research

Volumn 93, Issue 2, 2011, Pages 133-140

  Crawford Downs, J ^a   Roberts, Michael D ^a   Sigal, Ian A ^a  

^a DEVERS EYE INSTITUTE   (United States)

Author keywords

Biomechanics; Extracellular matrix; Glaucoma; Intraocular pressure; Lamina cribrosa; Optic nerve head; Remodeling

Indexed keywords

ARTICLE; ASTROCYTE; BIOMECHANICS; DISEASE COURSE; EXTRACELLULAR MATRIX; EYE; GLAUCOMA; HUMAN; INTRAOCULAR PRESSURE; LAMINA CRIBROSA; NONHUMAN; PRIORITY JOURNAL; RETINA GANGLION CELL; SIGNAL TRANSDUCTION;

ANIMALS; ASTROCYTES; AXONS; BIOMECHANICS; CONNECTIVE TISSUE; EXTRACELLULAR MATRIX; GLAUCOMA, OPEN-ANGLE; HUMANS; INTRAOCULAR PRESSURE; OPTIC DISK; OPTIC NERVE DISEASES; RETINAL GANGLION CELLS;

EID: 80052789462     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2010.08.004     Document Type: Article

References (57)

1. Agapova O.A., Kaufman P.L., Lucarelli M.J., Gabelt B.T., Hernandez M.R. Differential expression of matrix metalloproteinases in monkey eyes with experimental glaucoma or optic nerve transection. Brain Res. 2003, 967(1-2):132-143.
2. Agoumi, Y., Sharpe, G.P., Hutchison, D.M., Nicolela, M.T., Artes, P.H. Chauhan, B.C.: Laminar and prelaminar tissue displacement during intraocular pressure elevation in glaucoma patients and healthy controls. Ophthalmology, in press, doi:10.1016/j.ophtha.2010.05.016.
3. Albon J., Purslow P.P., Karwatowski W.S., Easty D.L. Age related compliance of the lamina cribrosa in human eyes. Br. J. Ophthalmol. 2000, 84(3):318-323.
4. Bellezza A.J., Hart R.T., Burgoyne C.F. The optic nerve head as a biomechanical structure: initial finite element modeling. Invest. Ophthalmol. Vis. Sci. 2000, 41(10):2991-3000.
5. Brown D.J., Morishige N., Neekhra A., Minckler D.S., Jester J.V. Application of second harmonic imaging microscopy to assess structural changes in optic nerve head structure ex vivo. J. Biomed. Opt. 2007, 12(2):024029.
6. Burgoyne C.F., Downs J.C. Premise and prediction-how optic nerve head biomechanics underlies the susceptibility and clinical behavior of the aged optic nerve head. J. Glaucoma 2008, 17(4):318-328.
7. Burgoyne C.F., Downs J.C., Bellezza A.J., Suh J.K., Hart R.T. 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. 2005, 24(1):39-73.
8. Downs J.C., Roberts M.D., Burgoyne C.F. Mechanical environment of the optic nerve head in glaucoma. Optom. Vis. Sci. 2008, 85(6):425-435.
9. Downs, J.C., Roberts, M.D., Burgoyne, C.F., Hart, R.T., 2009. Multiscale finite element modeling of the lamina cribrosa microarchitecture in the eye. In: Conf. Proc. IEEE Eng. Med. Biol. Soc., pp. 4277-4280.
10. Edwards M.E., Good T.A. Use of a mathematical model to estimate stress and strain during elevated pressure induced lamina cribrosa deformation. Curr. Eye Res. 2001, 23(3):215-225.
11. Edwards M.E., Wang S.S., Good T.A. Role of viscoelastic properties of differentiated SH-SY5Y human neuroblastoma cells in cyclic shear stress injury. Biotechnol. Prog. 2001, 17(4):760-767.
12. Grytz R., Meschke G. A computational remodeling approach to predict the physiological architecture of the collagen fibril network in corneo-scleral shells. Biomech. Model. Mechanobiol. 2009.
13. Hernandez M.R. Ultrastructural immunocytochemical analysis of elastin in the human lamina cribrosa. Changes in elastic fibers in primary open-angle glaucoma. Invest. Ophthalmol. Vis. Sci. 1992, 33(10):2891-2903.
14. Hernandez M.R. The optic nerve head in glaucoma: role of astrocytes in tissue remodeling. Prog. Retin. Eye Res. 2000, 19(3):297-321.
15. Irnaten M., Barry R.C., Quill B., Clark A.F., Harvey B.J., O'Brien C.J. Activation of stretch-activated channels and maxi-K+ channels by membrane stress of human lamina cribrosa cells. Invest. Ophthalmol. Vis. Sci. 2009, 50(1):194-202.
16. Jonas J.B., Berenshtein E., Holbach L. Lamina cribrosa thickness and spatial relationships between intraocular space and cerebrospinal fluid space in highly myopic eyes. Invest. Ophthalmol. Vis. Sci. 2004, 45(8):2660-2665.
17. Kagemann L., Ishikawa H., Wollstein G., Brennen P.M., Townsend K.A., Gabriele M.L., Schuman J.S. Ultrahigh-resolution spectral domain optical coherence tomography imaging of the lamina cribrosa. Ophthal. Surg. Lasers Imag. 2008, 39(Suppl. 4):S126-S131.
18. Kirwan R.P., Crean J.K., Fenerty C.H., Clark A.F., O'Brien C.J. Effect of cyclical mechanical stretch and exogenous transforming growth factor-beta1 on matrix metalloproteinase-2 activity in lamina cribrosa cells from the human optic nerve head. J. Glaucoma 2004, 13(4):327.
19. Kirwan R.P., Fenerty C.H., Crean J.K., Wordinger R.J., Clark A.F., O'Brien C.J. Influence of cyclical mechanical strain on extracellular matrix gene expression in human lamina cribrosa cells in vitro. Mol. Vis. 2005, 11:798-810.
20. LaPlaca M.C., Cullen D.K., McLoughlin J.J., Cargill R.S. High rate shear strain of three-dimensional neural cell cultures: a new in vitro traumatic brain injury model. J. Biomech. 2005, 38(5):1093-1105.
21. Leske M.C., Heijl A., Hussein M., Bengtsson B., Hyman L., Komaroff E. Factors for glaucoma progression and the effect of treatment: the early manifest glaucoma trial. Arch. Ophthalmol. 2003, 121(1):48-56.
22. Levy N.S., Crapps E.E. Displacement of optic nerve head in response to short-term intraocular pressure elevation in human eyes. Arch. Ophthalmol. 1984, 102(5):782-786.
23. Morgan J.E. Optic nerve head structure in glaucoma: astrocytes as mediators of axonal damage. Eye 2000, 14(Pt 3B):437-444.
24. Morrison J.C. Integrins in the optic nerve head: potential roles in glaucomatous optic neuropathy (an American Ophthalmological Society thesis). Trans. Am. Ophthalmol. Soc. 2006, 104:453-477.
25. O'Brien C., Butt Z., Ludlam C., Detkova P. Activation of the coagulation cascade in untreated primary open-angle glaucoma. Ophthalmology 1997, 104(4):725-729. discussion 729-730.
26. Oyama T., Abe H., Ushiki T. The connective tissue and glial framework in the optic nerve head of the normal human eye: light and scanning electron microscopic studies. Arch. Histol. Cytol. 2006, 69(5):341-356.
27. Pedersen J.A., Swartz M.A. Mechanobiology in the third dimension. Ann. Biomed. Eng. 2005, 33(11):1469-1490.
28. Pena J.D., Netland P.A., Vidal I., Dorr D.A., Rasky A., Hernandez M.R. Elastosis of the lamina cribrosa in glaucomatous optic neuropathy. Exp. Eye Res. 1998, 67(5):517-524.
29. Poostchi A., Wong T., Chan K.C., Kedzlie L., Sachdev N., Nicholas S., Garway-Heath D.F., Wells A.P. Optic disc diameter increases during acute elevations of intraocular pressure. Invest. Ophthalmol. Vis. Sci. 2010, 51(5):2313-2316.
30. Quigley H.A. Glaucoma: macrocosm to microcosm the Friedenwald lecture. Invest. Ophthalmol. Vis. Sci. 2005, 46(8):2662-2670.
31. Radius R.L. Anatomy of the optic nerve head and glaucomatous optic neuropathy. Surv. Ophthalmol. 1987, 32(1):35-44.
32. Ren R., Wang N., Li B., Li L., Gao F., Xu X., Jonas J.B. Lamina cribrosa and peripapillary sclera histomorphometry in normal and advanced glaucomatous Chinese eyes with various axial length. Invest. Ophthalmol. Vis. Sci. 2009, 50(5):2175-2184.
33. Roberts M.D., Grau V., Grimm J., Reynaud J., Bellezza A.J., Burgoyne C.F., Downs J.C. Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2009, 50(2):681-690.
34. Roberts, M.D., Hart, R.T., Liang, Y., Bellezza, A., Burgoyne, C.F., Downs, J., 2007. Continuum-level finite element modeling of the optic nerve head using a fabric tensor based description of the lamina cribrosa. In ASME Summer Bioengineering Conference. Keystone, Colorado.
35. Roberts M.D., Liang Y., Sigal I.A., Grimm J., Reynaud J., Bellezza A., Burgoyne C.F., Downs J.C. Correlation between local stress and strain and lamina cribrosa connective tissue volume fraction in normal monkey eyes. Invest. Ophthalmol. Vis. Sci. 2010, 51(1):295-307.
36. Roberts, M.D., Sigal, I.A., Liang, Y., Burgoyne, C.F., Downs, J.C. Changes in the biomechanical response of the optic nerve head in early experimental glaucoma. Invest. Ophthalmol. Vis. Sci., in press, doi:10.1167/iovs.10-5411.
37. Rogers, R., Ackloo, S., Dharsee, M., Flanagan, J.G., 2010. Biomarkers in response to biomechanical stress from human optic nerve head astrocytes. In: ARVO, Ft. Lauderdale, E-Abstract 2184.
38. Ruberti J.W., Hallab N.J. Strain-controlled enzymatic cleavage of collagen in loaded matrix. Biochem. Biophys. Res. Commun. 2005, 336(2):483-489.
39. Sander, E.A., Downs, J.C., Hart, R.T., Burgoyne, C.F., Nauman, E.A., 2006. In-plane mechanics of the optic nerve head with cellular solids models. In: World Congress of Biomechanics, Munich, Germany.
40. Sigal I.A. Interactions between geometry and mechanical properties on the optic nerve head. Invest. Ophthalmol. Vis. Sci. 2009, 50(6):2785-2795.
41. Sigal I.A., Ethier C.R. Biomechanics of the optic nerve head. Exp. Eye Res. 2009, 88(4):799-807.
42. Sigal I.A., Flanagan J.G., Ethier C.R. Factors influencing optic nerve head biomechanics. Invest. Ophthalmol. Vis. Sci. 2005, 46(11):4189-4199.
43. Sigal I.A., Flanagan J.G., Tertinegg I., Ethier C.R. Predicted extension, compression and shearing of optic nerve head tissues. Exp. Eye Res. 2007, 85(3):312-322.
44. Sigal I.A., Flanagan J.G., Tertinegg I., Ethier C.R. Modeling individual-specific human optic nerve head biomechanics. Part I: IOP-induced deformations and influence of geometry. Biomech. Model. Mechanobiol. 2009, 8(2):85-98.
45. Sigal I.A., Flanagan J.G., Tertinegg I., Ethier C.R. Modeling individual-specific human optic nerve head biomechanics. Part II: influence of material properties. Biomech. Model. Mechanobiol. 2009, 8(2):99-109.
46. Sigal I.A., Flanagan J.G., Tertinegg I., Ethier C.R. 3D morphometry of the human optic nerve head. Exp. Eye Res. 2010, 90(1):70-80.
47. Sigal I.A., Roberts M.D., Girard M., Burgoyne C.F., Downs J.C. Biomechanical changes of the optic disc. Ocular Disease: Mechanisms and Management 2010, Elsevier, New York. L.A. Levin, D.M. Albert (Eds.).
48. Sigal, I.A., Yang, H., Roberts, M.D., Grimm, J., Burgoyne, C.F., Downs, J.C., 2010c. Application of morphing methods to parameterize specimen-specific models and identify the main factors driving the biomechanics of the optic nerve head, 6th World Congress on Biomechanics, Singapore, August 1-6, 2010.
49. Sigal, I.A., Yang, H., Roberts, M.D., Grimm, J., Burgoyne, C.F., Downs, J.C., 2010d. Deformation of the lamina cribrosa and expansion of the scleral canal due to IOP elevation. A parametric study using eye-specific models, Association for Research in Vision and Ophthalmology (ARVO) Annual Meeting, Ft. Lauderdale, May 2 - May 6, 2010, IOVS 2010 51:E-abstract 2119.
50. Tan J.C., Kalapesi F.B., Coroneo M.T. Mechanosensitivity and the eye: cells coping with the pressure. Br. J. Ophthalmol. 2006, 90(3):383-388.
51. Wang J.H., Thampatty B.P. An introductory review of cell mechanobiology. Biomech. Model. Mechanobiol. 2006, 5(1):1-16.
52. Wells A.P., Garway-Heath D.F., Poostchi A., Wong T., Chan K.C., Sachdev N. Corneal hysteresis but not corneal thickness correlates with optic nerve surface compliance in glaucoma patients. Invest. Ophthalmol. Vis. Sci. 2008, 49(8):3262-3268.
53. Yang H., Downs J.C., Bellezza A., Thompson H., Burgoyne C.F. 3-D histomorphometry of the normal and early glaucomatous monkey optic nerve head: prelaminar neural tissues and cupping. Invest. Ophthalmol. Vis. Sci. 2007, 48(11):5068-5084.
54. Yang H., Downs J.C., Girkin C., Sakata L., Bellezza A., Thompson H., Burgoyne C.F. 3-D histomorphometry of the normal and early glaucomatous monkey optic nerve head: lamina cribrosa and peripapillary scleral position and thickness. Invest. Ophthalmol. Vis. Sci. 2007, 48(10):4597-4607.
55. Yang H., Downs J.C., Sigal I.A., Roberts M.D., Thompson H., Burgoyne C.F. Deformation of the normal monkey optic nerve head connective tissue after acute IOP elevation within 3-D histomorphometric reconstructions. Invest. Ophthalmol. Vis. Sci. 2009, 50(12):5785-5799.
56. Yang, H., Williams, G., Downs, J., Sigal, I.A., Roberts, M.D., Grimm, J., Thompson, H., Burgoyne, C., 2010. Optic nerve head (ONH) lamina cribrosa insertion migration and pialization in early non-human primate (NHP) experimental glaucoma. In ARVO, Ft. Lauderdale, E-Abstract 1631.
57. Zeimer R.C. Biomechanical properties of the optic nerve head. Optic Nerve in Glaucoma 1995, 107-121. Kugler Publications, Amsterdam. S.M. Drance, D.R. Anderson (Eds.).