Korean J Ophthalmol.  2018 Dec;32(6):470-477. 10.3341/kjo.2018.0015.

Relationship between Progressive Changes in Lamina Cribrosa Depth and Deterioration of Visual Field Loss in Glaucomatous Eyes

• Kim YN
• Shin JW
• Sung KR

• KMID: 2427961
• DOI: http://doi.org/10.3341/kjo.2018.0015

Abstract

PURPOSE
To investigate the relationship between the progression of visual field (VF) loss and changes in lamina cribrosa depth (LCD) as determined by spectral-domain optical coherence tomography (SD-OCT) enhanced depth imaging in patients with primary open angle glaucoma (POAG).
METHODS
Data from 60 POAG patients (mean follow-up, 3.5 ± 0.7 years) were included in this retrospective study. The LCD was measured in the optic disc image using SD-OCT enhanced depth imaging scanning at each visit. Change in the LCD was considered to either "˜increase' or "˜decrease' when the differences between baseline and the latest two consecutive follow-up visits were greater than the corresponding reproducibility coefficient value (23.08 µm, as determined in a preliminary reproducibility study). All participants were divided into three groups: increased LCD (ILCD), decreased LCD (DLCD), and no LCD change (NLCD). The Early Manifest Glaucoma Trial criteria were used to define VF deterioration. Kaplan-Meier survival analysis and Cox's proportional hazard models were performed to explore the relationship between VF progression and LCD change.
RESULTS
Of the 60 eyes examined, 35.0% (21 eyes), 28.3% (17 eyes), and 36.7% (22 eyes) were classified as the ILCD, DLCD, and NLCD groups, respectively. Kaplan-Meier survival analysis showed a greater cumulative probability of VF progression in the ILCD group than in the NLCD (p < 0.001) or DLCD groups (p = 0.018). Increased LCD was identified as the only risk factor for VF progression in the Cox proportional hazard models (hazard ratio, 1.008; 95% confidence interval, 1.000 to 1.015; p = 0.047).
CONCLUSIONS
Increased LCD was associated with a greater possibility of VF progression. The quantitative measurement of LCD changes, determined by SD-OCT, is a potential biomarker for the prediction of VF deterioration in patients with POAG.

Keyword

Glaucoma; Lamina cribrosa; Optic disk; Optical coherence tomography; Visual fields

MeSH Terms

Follow-Up Studies
Glaucoma
Glaucoma, Open-Angle
Humans
Optic Disk
Proportional Hazards Models
Retrospective Studies
Risk Factors
Tomography, Optical Coherence
Visual Fields*

Figure

• 

  Fig. 1 Measurement of lamina cribrosa depth (LCD) by spectral-domain optical coherence tomography. (A) En-face images of the optic nerve head were obtained from spectral-domain optical coherence tomography enhanced depth imaging scanning. Among several B-scans from optic disc scanning, a horizontal section image passing through major vessel trunks was selected to measure the LCD. This image-selecting procedure was repeated in the same eye at each follow up visit. (B) A line connecting the Bruch's membrane opening (red dots) on each side was regarded as the Bruch's membrane opening plane. The anterior surface of the lamina cribrosa was set as the horizontal margin, where the highly reflective region beneath the optic disc cup started. The distance of the three perpendicular lines (composed of the maximally depressed point, yellow arrow) from the reference line, and 100 and 200 µm apart from the maximally depressed point to temporal direction, were measured. A manual caliper tool and regions of interest manager of ImageJ software was used for each measurement and the LCD was determined by the average value measured from the three points.

• 

  Fig. 2 Subgroup analysis of lamina cribrosa displacement. The method of measuring lamina cribrosa depth (LCD) described in Fig. 1 was repeated at each follow-up visit. The values were determined at each follow-up visit and the difference from the first to the last measurement was considered LCD change. A significant LCD change was defined as a value greater, within and less than the reproducibility coefficient (23.08 µm). (A) Posteriorly displaced lamina cribrosa (LC), (B) no significant LC displacement, and (C) anteriorly displaced LC.

• 

  Fig. 3 Kaplan-Meier estimates of visual field progression during the follow up period. X-axis, follow-up period (year); Y-axis, cumulative probability of the visual field progression. *p< 0.05 considered as statistically significant. LCD = lamina cribrosa depth; ILCD = increased LCD; NLCD = no LCD change; DLCD = decreased LCD.

Reference

1. 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; 99:635–649.

2. Quigley HA, Anderson DR. Distribution of axonal transport blockade by acute intraocular pressure elevation in the primate optic nerve head. Invest Ophthalmol Vis Sci. 1977; 16:640–644.

3. Radius RL, Anderson DR. Rapid axonal transport in primate optic nerve. Distribution of pressure-induced interruption. Arch Ophthalmol. 1981; 99:650–654.

4. Kim TW, Kagemann L, Girard MJ, et al. Imaging of the lamina cribrosa in glaucoma: perspectives of pathogenesis and clinical applications. Curr Eye Res. 2013; 38:903–909.

5. 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; 5:1114–1123.

6. Vilupuru AS, Rangaswamy NV, Frishman LJ, et al. Adaptive optics scanning laser ophthalmoscopy for in vivo imaging of lamina cribrosa. J Opt Soc Am A Opt Image Sci Vis. 2007; 24:1417–1425.

7. Chung HS, Sung KR, Lee KS, et al. Relationship between the lamina cribrosa, outer retina, and choroidal thickness as assessed using spectral domain optical coherence tomography. Korean J Ophthalmol. 2014; 28:234–240.

8. Burgoyne CF, Downs JC. Premise and prediction-how optic nerve head biomechanics underlies the susceptibility and clinical behavior of the aged optic nerve head. J Glaucoma. 2008; 17:318–328.

9. Yang H, Downs JC, Bellezza A, et al. 3-D histomorphometry of the normal and early glaucomatous monkey optic nerve head: prelaminar neural tissues and cupping. Invest Ophthalmol Vis Sci. 2007; 48:5068–5084.

10. 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; 54:4836–4842.

11. Xu G, Weinreb RN, Leung CK. Optic nerve head deformation in glaucoma: the temporal relationship between optic nerve head surface depression and retinal nerve fiber layer thinning. Ophthalmology. 2014; 121:2362–2370.

12. Lee EJ, Kim TW, Kim M, Kim H. Influence of lamina cribrosa thickness and depth on the rate of progressive retinal nerve fiber layer thinning. Ophthalmology. 2015; 122:721–729.

13. Omodaka K, Takahashi S, Matsumoto A, et al. Clinical factors associated with lamina cribrosa thickness in patients with glaucoma, as measured with swept source optical coherence tomography. PLoS One. 2016; 11:e0153707.

14. Chung HS, Sung KR, Lee JY, Na JH. Lamina cribrosa-related parameters assessed by optical coherence tomography for prediction of future glaucoma progression. Curr Eye Res. 2016; 41:806–813.

15. Lee EJ, Kim TW, Weinreb RN. Reversal of lamina cribrosa displacement and thickness after trabeculectomy in glaucoma. Ophthalmology. 2012; 119:1359–1366.

16. Kim S, Sung KR, Lee JR, Lee KS. Evaluation of lamina cribrosa in pseudoexfoliation syndrome using spectral-domain optical coherence tomography enhanced depth imaging. Ophthalmology. 2013; 120:1798–1803.

17. Vaz S, Falkmer T, Passmore AE, et al. The case for using the repeatability coefficient when calculating test-retest reliability. PLoS One. 2013; 8:e73990.

18. Heijl A, Leske MC, Bengtsson B, et al. Measuring visual field progression in the Early Manifest Glaucoma Trial. Acta Ophthalmol Scand. 2003; 81:286–293.

19. Lee EJ, Kim TW, Weinreb RN, et al. Three-dimensional evaluation of the lamina cribrosa using spectral-domain optical coherence tomography in glaucoma. Invest Ophthalmol Vis Sci. 2012; 53:198–204.

20. Bellezza AJ, Rintalan CJ, Thompson HW, et al. Anterior scleral canal geometry in pressurised (IOP 10) and non-pressurised (IOP 0) normal monkey eyes. Br J Ophthalmol. 2003; 87:1284–1290.

21. Vianna JR, Lanoe VR, Quach J, et al. Serial changes in lamina cribrosa depth and neuroretinal parameters in glaucoma: impact of choroidal thickness. Ophthalmology. 2017; 124:1392–1402.

22. Faridi OS, Park SC, Kabadi R, et al. Effect of focal lamina cribrosa defect on glaucomatous visual field progression. Ophthalmology. 2014; 121:1524–1530.

23. Minckler DS, Bunt AH, Johanson GW. Orthograde and retrograde axoplasmic transport during acute ocular hypertension in the monkey. Invest Ophthalmol Vis Sci. 1977; 16:426–441.

24. Quigley HA, Addicks EM. Regional differences in the structure of the lamina cribrosa and their relation to glaucomatous optic nerve damage. Arch Ophthalmol. 1981; 99:137–143.

25. Sigal IA, Flanagan JG, Tertinegg I, Ethier CR. Predicted extension, compression and shearing of optic nerve head tissues. Exp Eye Res. 2007; 85:312–322.

26. Reis AS, O'Leary N, Stanfield MJ, et al. Laminar displacement and prelaminar tissue thickness change after glaucoma surgery imaged with optical coherence tomography. Invest Ophthalmol Vis Sci. 2012; 53:5819–5826.

27. Lee EJ, Kim TW, Weinreb RN, Kim H. Reversal of lamina cribrosa displacement after intraocular pressure reduction in open-angle glaucoma. Ophthalmology. 2013; 120:553–559.

28. Sigal IA, Yang H, Roberts MD, et al. IOP-induced lamina cribrosa displacement and scleral canal expansion: an analysis of factor interactions using parameterized eye-specific models. Invest Ophthalmol Vis Sci. 2011; 52:1896–1907.

29. Chakraborty R, Read SA, Collins MJ. Diurnal variations in axial length, choroidal thickness, intraocular pressure, and ocular biometrics. Invest Ophthalmol Vis Sci. 2011; 52:5121–5129.

30. Rho CR, Park HY, Lee NY, Park CK. Clock-hour laminar displacement and age in primary open-angle glaucoma and normal tension glaucoma. Clin Exp Ophthalmol. 2012; 40:e183–e189.