Lamina cribrosa position and Bruch’s membrane opening differences between anterior ischemic optic neuropathy and open-angle glaucoma

Abstract

Purpose:

To compare the optic nerve head morphology among primary open-angle glaucoma, non-arteritic anterior ischemic optic neuropathy eyes, their fellow healthy eyes and control eyes, using spectral-domain optical coherence tomography with enhanced depth imaging.

Methods:

Observational cross-sectional study including 88 eyes of 68 patients. In this study, 23 non-arteritic anterior ischemic optic neuropathy eyes, 17 fellow unaffected eyes, 25 primary open-angle glaucoma eyes, and 23 age-matched control eyes were included. Peripapillary retinal nerve fiber layer thickness and optic disk area were evaluated. Bruch’s membrane opening diameter, optic cup depth, anterior lamina cribrosa depth, and prelaminar tissue thickness were assessed.

Results:

Non-arteritic anterior ischemic optic neuropathy and primary open-angle glaucoma eyes had similar visual field mean deviation and peripapillary retinal nerve fiber layer thickness (P = 0.6 and P = 0.56, respectively). Bruch’s membrane opening diameter was significantly larger in primary open-angle glaucoma eyes than in control eyes (P = 0.02). Lamina cribrosa and disk cup were deeper in eyes with primary open-angle glaucoma than both control and non-arteritic anterior ischemic optic neuropathy eyes (P < 0.001). Prelaminar tissue thickness was significantly thinner in primary open-angle glaucoma eyes than in non-arteritic anterior ischemic optic neuropathy eyes (P < 0.001). Lamina cribrosa was shallower in both non-arteritic anterior ischemic optic neuropathy and unaffected fellow eyes compared to healthy eyes (P < 0.001 and P = 0.04, respectively). No differences were found in the optic disk area.

Conclusion:

A forward lamina cribrosa placement and not a smaller disk could be involved in the pathogenesis of non-arteritic anterior ischemic optic neuropathy. A significantly larger Bruch’s membrane opening diameter was found in primary open-angle glaucoma eyes compared with control eyes. This issue has clinical implications because Bruch’s membrane opening has been considered a stable reference for disk-related measures.

Keywords

Bruch’s membrane opening diameter lamina cribrosa non-arteritic anterior ischemic optic neuropathy optic disk area primary open-angle glaucoma

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References

Gaasterland

Tanishima

Kuwabara

. Axoplasmic flow during chronic experimental glaucoma. 1. Light and electron microscopic studies of the monkey optic nervehead during development of glaucomatous cupping. Invest Ophthalmol Vis Sci 1978; 17: 838–846.

Minckler

Bunt

Johanson

. Orthograde and retrograde axoplasmic transport during acute ocular hypertension in the monkey. Invest Ophthalmol Vis Sci 1977; 16: 426–441.

Quigley

Addicks

Green

et al . Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage. Arch Ophthalmol 1981; 99: 635–649.

Quigley

Green

. The histology of human glaucoma cupping and optic nerve damage: clinicopathologic correlation in 21 eyes. Ophthalmology 1979; 86: 1803–1830.

Bellezza

Rintalan

Thompson

et al . Deformation of the lamina cribrosa and anterior scleral canal wall in early experimental glaucoma. Invest Ophthalmol Vis Sci 2003; 44: 623–637.

Morgan-Davies

Taylor

Hill

et al . Three dimensional analysis of the lamina cribrosa in glaucoma. Br J Ophthalmol 2004; 88(10): 1299–1304.

Roberts

Burgoyne

. Mechanical environment of the optic nerve head in glaucoma. Optom Vis Sci 2008; 85(6): 425–435.

Anderson

Hendrickson

. Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve. Invest Ophthalmol 1974; 13: 771–783.

Minckler

Tso

. A light microscopic, autoradiographic study of axoplasmic transport in the normal rhesus optic nerve head. Am J Ophthalmol 1976; 82: 1–15.

10.

Hernandez

. The optic nerve head in glaucoma: role of astrocytes in tissue remodeling. Prog Retin Eye Res 2000; 19: 297–321.

11.

Hayreh

. The blood supply of the optic nerve head and the evaluation of it—myth and reality. Prog Retin Eye Res 2001; 20: 563–593.

12.

Fard

Afzali

Abdi

et al . Comparison of the pattern of macular ganglion cell-inner plexiform layer defect between ischemic optic neuropathy and open-angle glaucoma. Invest Ophthalmol Vis Sci 2016; 57(3): 1011–1016.

13.

Yeoh

Rahman

Chen

et al . Choroidal imaging in inherited retinal disease using the technique of enhanced depth imaging optical coherence tomography. Graefes Arch Clin Exp Ophthalmol 2010; 248(12): 1719–1728.

14.

Dell’Omo

Costagliola

Di Salvatore

et al . Enhanced depth imaging spectral-domain optical coherence tomography. Retina 2010; 30(2): 378–379.

15.

Zlotnik

Ben-Yaish

Zalevsky

. Extending the depth of focus for enhanced three-dimensional imaging and profilometry: an overview. Appl Opt 2009; 48: H105–H112.

16.

Fujiwara

Imamura

Margolis

et al . Enhanced depth imaging optical coherence tomography of the choroid in highly myopic eyes. Am J Ophthalmol 2009; 148(3): 445–450.

17.

Margolis

Spaide

. A pilot study of enhanced depth imaging optical coherence tomography of the choroid in normal eyes. Am J Ophthalmol 2009; 147: 811–815.

18.

Furlanetto

Park

Damle

et al . Posterior displacement of the lamina cribrosa in glaucoma: in vivo interindividual and intereye comparisons. Invest Ophthalmol Vis Sci 2013; 54(7): 4836–4842.

19.

Park

Jeon

Park

. Enhanced depth imaging detects lamina cribrosa thickness differences in normal tension glaucoma and primary open-angle glaucoma. Ophthalmology 2012; 119: 10–20.

20.

Weinreb

et al . Optic nerve head deformation in glaucoma: a prospective analysis of optic nerve head surface and lamina cribrosa surface displacement. Ophthalmology 2015; 122(7): 1317–1329.

21.

Lin

Crowther

et al . Impact of rates of change of lamina cribrosa and optic nerve head surface depths on visual field progression in glaucoma. Invest Ophthalmol Vis Sci 2017; 58(3): 1825–1833.

22.

Fard

Afzali

Abdi

et al . Optic nerve head morphology in nonarteritic anterior ischemic optic neuropathy compared to open-angle glaucoma. Invest Ophthalmol Vis Sci 2016; 57: 4632–4640.

23.

Lee

Choi

Kim

T-W

et al . Comparison of the deep optic nerve head structure between normal-tension glaucoma and nonarteritic anterior ischemic optic neuropathy. PLoS ONE 2016; 11(4): e0150242.

24.

Rebolleda

Puerto

de Juan

et al . Optic nerve head biomechanic and IOP changes before and after the injection of aflibercept for neovascular age-related macular degeneration. Invest Ophthalmol Vis Sci 2016; 57: 5688–5695.

25.

Yang

Hou

et al . Optic neuropathy induced by experimentally reduced cerebrospinal fluid pressure in monkeys. Invest Ophthalmol Vis Sci 2014; 55(5): 3067–3073.

26.

Yang

Ren

Lockwood

et al . The connective tissue components of optic nerve head cupping in monkey experimental glaucoma part 1: global change. Invest Ophthalmol Vis Sci 2015; 56(13): 7661–7678.

27.

Lee

Kim

T-W

Weinreb

et al . Visualization of the lamina cribrosa using enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 2011; 152(1): 87–95.

28.

Park

De Moraes

CGV

Teng

et al . Enhanced depth imaging optical coherence tomography of deep optic nerve complex structures in glaucoma. Ophthalmology 2012; 119: 3–9.

29.

Berdahl

Allingham

. Intracranial pressure and glaucoma. Curr Opin Ophthalmol 2010; 21: 106–111.

30.

Lee

Kim

T-W

Weinreb

. Reversal of lamina cribrosa displacement and thickness after trabeculectomy in glaucoma. Ophthalmology 2012; 119: 1359–1366.

31.

Barrancos

Rebolleda

Oblanca

et al . Changes in lamina cribrosa and prelaminar tissue after deep sclerectomy 2014; 28(1): 58–65.

32.

Bowd

Weinreb

Lee

et al . Optic disk topography after medical treatment to reduce intraocular pressure. Am J Ophthalmol 2000; 130: 280–286.

33.

Lucy

Wang

Schyman

et al . Thck prelaminar tissue decreases lamina cribrosa visibility. Invest Ophthalmol Vis Sci 2017; 158(3): 1751–1757.

34.

Gardiner

Boey

Yang

et al . Structural measurements for monitoring change in glaucoma: comparing retinal nerve fiber layer thickness with minimum rim width and area. Invest Ophthalmol Vis Sci 2015; 56: 6886–6891.

35.

Danesh-Meyer

Boland

Savino

et al . Optic disc morphology in open-angle glaucoma compared with anterior ischemic optic neuropathies. Invest Ophthalmol Vis Sci 2010; 51: 2003–2010.

36.

Rebolleda

García-Montesinos

De Dompablo

et al . Bruch’s membrane opening changes and lamina cribrosa displacement in non-arteritic anterior ischaemic optic neuropathy. Br J Ophthalmol 2017; 101(2): 143–149.

37.

Fard

Abdi

Kasaei

et al . Peripapillary choroidal thickness in nonarteritic anterior ischemic optic neuropathy. Invest Ophthalmol Vis Sci 2015; 56: 3027–3033.

38.

Mansour

Shoch

Logani

. Optic disk size in ischemic optic neuropathy. Am J Ophthalmol 1988; 106(5): 587–589.

39.

Jonas

Gusek

Naumann

. Anterior ischemic optic neuropathy: nonarteritic form in small and giant cell arteritis in normal sized optic discs. Int Ophthalmol 1988; 12(2): 119–125.

40.

Contreras

Rebolleda

Noval

et al . Optic disc evaluation by optical coherence tomography in nonarteritic anterior ischemic optic neuropathy. Invest Ophthalmol Vis Sci 2007; 48: 4087–4092.

41.

Reis

O’Leary

Yang

et al . Influence of clinically invisible, but optical coherence tomography detected, optic disc margin anatomy on neuroretinal rim evaluation. Invest Ophthalmol Vis Sci 2012; 53: 1852–1860.

42.

Nagia

Huisingh

Johnstone

et al . Peripapillary pachychoroid in nonarteritic anterior ischemic optic neuropathy. Invest Ophthalmol Vis Sci 2016; 57(11): 4679–4685.

43.

Pérez-Sarriegui

Muñoz-Negrete

Noval

et al . Automated evaluation of choroidal thickness and minimum rim width thickness in nonarteritic ischaemic optic neuropathy. J Neuroophthalmol 2018; 38: 7–12.

44.

Rhodes

Huisingh

Johnstone

et al . Peripapillary choroidal thickness variation with age and race in normal eyes. Invest Ophthalmol Vis Sci 2015; 56(3): 1872–1879.

45.

Vianna

Lanoe

Quach

et al . Serial changes in lamina cribrosa depth and neuroretinal parameters in glaucoma: impact of choroidal thickness. Ophthalmology 2017; 124: 1392–1402.