Abstract
The lamina cribrosa is the putative site of retinal ganglion cell axonal injury in glaucoma. Although histological studies have provided evidence of structural changes to the lamina cribrosa, even in early stages of glaucoma, until recently, the ability to evaluate the lamina cribrosa in vivo has been limited. Recent advances in optical coherence tomography, including enhanced depth and swept-source imaging, have changed this, providing a means to image the lamina cribrosa. Imaging has identified general and localized configurational changes in the lamina of glaucomatous eyes, including posterior laminar displacement, altered laminar thickness, and focal laminar defects with spatial association with conventional structural and functional losses. In addition, although the temporal relationship between changes to the lamina cribrosa and glaucomatous retinal ganglion cell loss is yet to be elucidated, quantitative measurements of laminar microarchitecture have good reproducibility and offer the potential to serve as biomarkers for glaucoma diagnosis and progression.
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References
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Weinreb RN, Aung T, Medeiros FA. The pathophysiology and treatment of glaucoma: a review. JAMA. 2014;311:1901–11.
Minckler DS, Bunt AH, Johanson GW. Orthograde and retrograde axoplasmic transport during acute ocular hypertension in the monkey. Invest Ophthalmol Vis Sci. 1977;16:426–41.
Quigley HA, Addicks EM. Regional differences in the structure of the lamina cribrosa and their relation to glaucomatous optic nerve damage. Arch Ophthalmol. 1981;99:137–43.
Quigley HA, Addicks EM, Green WR, Maumenee AE. Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage. Arch Ophthalmol. 1981;99:635–49.
Burgoyne CF, Downs JC, Bellezza AJ, Hart RT. Three-dimensional reconstruction of normal and early glaucoma monkey optic nerve head connective tissues. Invest Ophthalmol Vis Sci. 2004;45:4388–99.
Kass MA, Heuer DK, Higginbotham EJ, et al. The Ocular Hypertension Treatment Study: a randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary open-angle glaucoma. Arch Ophthalmol. 2002;120:701–13 discussion 829–30.
Anderson DR, Drance SM, Schulzer M, Group CN-TGS. Factors that predict the benefit of lowering intraocular pressure in normal tension glaucoma. Am J Ophthalmol. 2003;136:820–9.
Anderson DR, Hendrickson A. Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve. Invest Ophthalmol. 1974;13:771–83.
Gamero GE, Fechtner RD. The optic nerve in glaucoma. In: Choplin NT, Lundy DC, editors. Atlas of Glaucoma. London: Informa Healthcare; 2007. p. 59–74.
Burgoyne CF. A biomechanical paradigm for axonal insult within the optic nerve head in aging and glaucoma. Exp Eye Res. 2011;93:120–32.
Anderson DR. Ultrastructure of human and monkey lamina cribrosa and optic nerve head. Arch Ophthalmol. 1969;82:800–14.
Jonas JB, Mardin CY, Schlötzer-Schrehardt U, Naumann GO. Morphometry of the human lamina cribrosa surface. Invest Ophthalmol Vis Sci. 1991;32:401–5.
Strouthidis NG, Girard MJ. Altering the way the optic nerve head responds to intraocular pressure-a potential approach to glaucoma therapy. Curr Opin Pharmacol. 2013;13:83–9.
Crawford Downs J, Roberts MD, Sigal IA. Glaucomatous cupping of the lamina cribrosa: a review of the evidence for active progressive remodeling as a mechanism. Exp Eye Res. 2011;93:133–40.
Burgoyne CF, Downs JC, Bellezza AJ, Suh JK, Hart RT. 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;24:39–73.
Burgoyne CF, Quigley HA, Thompson HW, Vitale S, Varma R. Early changes in optic disc compliance and surface position in experimental glaucoma. Ophthalmology. 1995;102:1800–9.
Yan DB, Coloma FM, Metheetrairut A, et al. Deformation of the lamina cribrosa by elevated intraocular pressure. Br J Ophthalmol. 1994;78:643–8.
Quigley HA, Hohman RM, Addicks EM, Massof RW, Green WR. Morphologic changes in the lamina cribrosa correlated with neural loss in open-angle glaucoma. Am J Ophthalmol. 1983;95:673–91.
Jonas JB, Berenshtein E, Holbach L. Anatomic relationship between lamina cribrosa, intraocular space, and cerebrospinal fluid space. Invest Ophthalmol Vis Sci. 2003;44:5189–95.
Morgan WH, Yu DY, Alder VA, et al. The correlation between cerebrospinal fluid pressure and retrolaminar tissue pressure. Invest Ophthalmol Vis Sci. 1998;39:1419–28.
The Advanced Glaucoma Intervention Study (AGIS). 12. Baseline risk factors for sustained loss of visual field and visual acuity in patients with advanced glaucoma. Am J Ophthalmol. 2002;134:499–512.
Ren R, Jonas JB, Tian G, et al. Cerebrospinal fluid pressure in glaucoma: a prospective study. Ophthalmology. 2010;117:259–66.
Huang D, Swanson EA, Lin CP, et al. Optical coherence tomography. Science. 1991;254:1178–81.
Wollstein G, Schuman JS, Price LL, et al. Optical coherence tomography longitudinal evaluation of retinal nerve fiber layer thickness in glaucoma. Arch Ophthalmol. 2005;123:464–70.
Medeiros FA, Zangwill LM, Bowd C, et al. Evaluation of retinal nerve fiber layer, optic nerve head, and macular thickness measurements for glaucoma detection using optical coherence tomography. Am J Ophthalmol. 2005;139:44–55.
Knight OJ, Chang RT, Feuer WJ, Budenz DL. Comparison of retinal nerve fiber layer measurements using time domain and spectral domain optical coherent tomography. Ophthalmology. 2009;116:1271–7.
Kagemann L, Ishikawa H, Wollstein G, et al. Ultrahigh-resolution spectral domain optical coherence tomography imaging of the lamina cribrosa. Ophthalmic Surg Lasers Imaging. 2008;39:S126–31.
Inoue R, Hangai M, Kotera Y, et al. Three-dimensional high-speed optical coherence tomography imaging of lamina cribrosa in glaucoma. Ophthalmology. 2009;116:214–22.
Strouthidis NG, Grimm J, Williams GA, et al. A comparison of optic nerve head morphology viewed by spectral domain optical coherence tomography and by serial histology. Invest Ophthalmol Vis Sci. 2010;51:1464–74.
Lin P, Mettu PS, Pomerleau DL, et al. Image inversion spectral-domain optical coherence tomography optimizes choroidal thickness and detail through improved contrast. Invest Ophthalmol Vis Sci. 2012;53:1874–82.
Spaide RF, Koizumi H, Pozzoni MC, Pozonni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol. 2008;146:496–500.
Rebolleda G, Muñoz Negrete FJ. Enhanced depth imaging—optical coherence tomography technique and the lamina cribrosa in glaucoma. Arch Soc Esp Oftalmol. 2014;89:133–5.
Park HY, Park CK. Diagnostic capability of lamina cribrosa thickness by enhanced depth imaging and factors affecting thickness in patients with glaucoma. Ophthalmology. 2013;120:745–52.
Leung CK. Diagnosing glaucoma progression with optical coherence tomography. Curr Opin Ophthalmol. 2014;25:104–11.
Yasuno Y, Hong Y, Makita S, et al. In vivo high-contrast imaging of deep posterior eye by 1-microm swept source optical coherence tomography and scattering optical coherence angiography. Opt Express. 2007;15:6121–39.
Srinivasan VJ, Adler DC, Chen Y, et al. Ultrahigh-speed optical coherence tomography for three-dimensional and en face imaging of the retina and optic nerve head. Invest Ophthalmol Vis Sci. 2008;49:5103–10.
Ivers KM, Li C, Patel N, et al. Reproducibility of measuring lamina cribrosa pore geometry in human and nonhuman primates with in vivo adaptive optics imaging. Invest Ophthalmol Vis Sci. 2011;52:5473–80.
Akagi T, Hangai M, Takayama K, et al. In vivo imaging of lamina cribrosa pores by adaptive optics scanning laser ophthalmoscopy. Invest Ophthalmol Vis Sci. 2012;53:4111–9.
Dreher AW, Bille JF, Weinreb RN. Active optical depth resolution improvement of the laser tomographic scanner. Appl Opt. 1989;28:804–8.
Liang J, Williams DR, Miller DT. Supernormal vision and high-resolution retinal imaging through adaptive optics. J Opt Soc Am A Opt Image Sci Vis. 1997;14:2884–92.
Miller DT, Kocaoglu OP, Wang Q, Lee S. Adaptive optics and the eye (super resolution OCT). Eye (Lond). 2011;25:321–30.
Park SC, Kiumehr S, Dorairaj S, et al. In-vivo, 3-dimensional imaging of the lamina cribrosa horizontal central ridge in normals and lamina cribrosa deformation in glaucoma. Invest Ophthalmol Vis Sci. 2011;52:3063 E-Abstract.
• Furlanetto RL, Park SC, Damle UJ, et al. Posterior displacement of the lamina cribrosa in glaucoma: in vivo interindividual and intereye comparisons. Invest Ophthalmol Vis Sci. 2013;54(7):4836–42. In vivo human study, showing that lamina cribrosa was located more posteriorly in glaucoma patients comparing to normal subjects.
Ren R, Yang H, Gardiner SK, et al. Anterior lamina cribrosa surface depth, age, and visual field sensitivity in the Portland Progression Project. Invest Ophthalmol Vis Sci. 2014;55:1531–9.
• Seo JH, Kim TW, Weinreb RN. Lamina cribrosa depth in healthy eyes. Invest Ophthalmol Vis Sci. 2014;55:1241–51. Study in normal eyes using EDI-OCT showing a wide variation in normal lamina cribrosa depth. The study also found correlation between lamina depth with axial length and gender.
Cheung CY, Chen D, Wong TY, et al. Determinants of quantitative optic nerve measurements using spectral domain optical coherence tomography in a population-based sample of non-glaucomatous subjects. Invest Ophthalmol Vis Sci. 2011;52:9629–35.
Kim TW, Kim M, Weinreb RN, et al. Optic disc change with incipient myopia of childhood. Ophthalmology. 2012;119:21–6 e1–3.
Jonas JB, 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;45:2660–5.
Burgoyne CF, Morrison JC. The anatomy and pathophysiology of the optic nerve head in glaucoma. J Glaucoma. 2001;10:S16–8.
Park HY, Jeon SH, Park CK. Enhanced depth imaging detects lamina cribrosa thickness differences in normal tension glaucoma and primary open-angle glaucoma. Ophthalmology. 2012;119:10–20.
Park HY, Shin HY, Park CK. Imaging the posterior segment of the eye using swept-source optical coherence tomography in myopic glaucoma eyes: comparison with enhanced-depth imaging. Am J Ophthalmol. 2014;157:550–7.
Kiumehr S, Park SC, Syril D, et al. In vivo evaluation of focal lamina cribrosa defects in glaucoma. Arch Ophthalmol. 2012;130:552–9.
You JY, Park SC, Su D, et al. Focal lamina cribrosa defects associated with glaucomatous rim thinning and acquired pits. JAMA Ophthalmol. 2013;131:314–20.
Tatham AJ, Miki A, Weinreb RN, Zangwill LM, Medeiros FA. Defects of the lamina cribrosa in eyes with localized retinal nerve fiber layer loss. Ophthalmology. 2014;121:110–8.
Park SC, Hsu AT, Su D, et al. Factors associated with focal lamina cribrosa defects in glaucoma. Invest Ophthalmol Vis Sci. 2013;54:8401–7.
Lee EJ, Kim TW, Kim M, et al. Recent structural alteration of the peripheral lamina cribrosa near the location of disc hemorrhage in glaucoma. Invest Ophthalmol Vis Sci. 2014;55:2805–15.
Faridi OS, Park SC, Kabadi R, et al. Effect of focal lamina cribrosa defect on glaucomatous visual field progression. Ophthalmology. 2014;121:1524–30.
Wilkins MR, Fitzke FW, Khaw PT. Pointwise linear progression criteria and the detection of visual field change in a glaucoma trial. Eye (Lond). 2006;20:98–106.
Maeda H, Nakamura M, Yamamoto M. Morphometric features of laminar pores in lamina cribrosa observed by scanning laser ophthalmoscopy. Jpn J Ophthalmol. 1999;43:415–21.
Miglior S, Rossetti L, Lonati C, Orzalesi N. Scanning laser ophthalmoscopy of the optic disc at the level of the lamina cribrosa. Curr Eye Res. 1998;17:453–61.
Miller KM, Quigley HA. The clinical appearance of the lamina cribrosa as a function of the extent of glaucomatous optic nerve damage. Ophthalmology. 1988;95:135–8.
Susanna R. The lamina cribrosa and visual field defects in open-angle glaucoma. Can J Ophthalmol. 1983;18:124–6.
Hermann B, Fernández EJ, Unterhuber A, et al. Adaptive-optics ultrahigh-resolution optical coherence tomography. Opt Lett. 2004;29:2142–4.
Zhang Y, Rha J, Jonnal R, Miller D. Adaptive optics parallel spectral domain optical coherence tomography for imaging the living retina. Opt Express. 2005;13:4792–811.
•• Nadler Z, Wang B, Wollstein G, et al. Automated lamina cribrosa microstructural segmentation in optical coherence tomography scans of healthy and glaucomatous eyes. Biomed Opt Express. 2013;4:2596–608. Study showing that automated segmentation algorithm for in vivo imaging of the lamina cribrosa was similar to manual segmentation with the advantage of providing faster imaging analysis.
Nadler Z, Wang B, Wollstein G, et al. Repeatability of in vivo 3D lamina cribrosa microarchitecture using adaptive optics spectral domain optical coherence tomography. Biomed Opt Express. 2014;5:1114–23.
Wang B, Nevins JE, Nadler Z, et al. In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography. Invest Ophthalmol Vis Sci. 2013;54:8270–4.
Wang B, Nevins JE, Nadler Z, et al. Reproducibility of in vivo OCT measured three-dimensional human lamina cribrosa microarchitecture. PLoS ONE. 2014;9:e95526.
Somfai GM, Salinas HM, Puliafito CA, Fernández DC. Evaluation of potential image acquisition pitfalls during optical coherence tomography and their influence on retinal image segmentation. J Biomed Opt. 2007;12:041209.
Acknowledgments
This article was supported in part by the National Institutes of Health/National Eye Institute grants EY021818 (F.A.M.), core grant P30EY022589; an unrestricted grant from Research to Prevent Blindness (New York, NY); fellowships from Brazilian National Research Council-CAPES 12309-13-3 (C.P.B.G.).
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Dr. Abe, Dr. Gracitelli, and Dr. Diniz-Filho declare they have no conflicts of interest to declare. Dr. Tatham declares they received research support from Heidelberg Engineering. Dr. Medeiros declares they received research support from Alcon Laboratories, Bausch & Lomb, Carl Zeiss Meditec, Heidelberg Engineering, Merck, Allergan, Sensimed, Topcon, Reichert, National Eye Institute; Consultant for Allergan, Carl Zeiss Meditec, Novartis.
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This article is part of the Topical Collection on Diagnosis and Monitoring of Glaucoma.
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Abe, R.Y., Gracitelli, C.P.B., Diniz-Filho, A. et al. Lamina Cribrosa in Glaucoma: Diagnosis and Monitoring. Curr Ophthalmol Rep 3, 74–84 (2015). https://doi.org/10.1007/s40135-015-0067-7
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DOI: https://doi.org/10.1007/s40135-015-0067-7