Association of Bergmeister Papilla and Deep Optic Nerve Head Structures With Prelaminar Schisis of Normal and Glaucomatous Eyes

Abstract

PURPOSE: To investigate factors associated with the severity of prelaminar schisis (PLS) in heathy subjects and glaucoma patients.DESIGN: Prospective cross-sectional study.METHODS: A total of 217 eyes of 217 subjects (110 normal eyes and 107 open angle glaucoma eyes) were studied. Frequency and severity of PLS were compared between normal and glaucomatous eyes. Multivariate logistic models were used to assess factors associated with the severity of PLS. Factors considered were age, axial length, glaucomatous damage indices, Bruch membrane opening (BMO) and anterior scleral canal opening parameters, tractional forces (posterior vitreous staging and presence of Bergmeister papilla), circumpapillary choroidal thickness, lamina cribrosa (LC) parameters, and peripapillary scleral (PPS) angle.RESULTS: The frequency of PLS was 70.9% in normal eyes and 72.0% in glaucomatous eyes. There was no difference in frequency and severity between the groups. The presence of Bergmeister papilla was the strongest predictor of a more severe PLS in both normal and glaucomatous eyes (odds ratio [OR] + 9.78, 12.5; both P < .001). A larger PPS angle in normal eyes (OR = 1.19; P = .003) and a larger BMO area and a deeper LC depth in glaucomatous eyes (OR = 1.08, 1.05; both P = .038) were associated with severity of PLS.CONCLUSIONS: The severity of PLS was strongly associated with the presence of Bergmeister papilla, suggesting a traction-related phenomenon. Correlation of PLS severity with larger BMO area and deeper LC depth, which are optic nerve head structures associated with glaucoma, suggested its possible relationship with glaucomatous damage. PURPOSE: To investigate factors associated with the severity of prelaminar schisis (PLS) in heathy subjects and glaucoma patients. DESIGN: Prospective cross-sectional study. METHODS: A total of 217 eyes of 217 subjects (110 normal eyes and 107 open angle glaucoma eyes) were studied. Frequency and severity of PLS were compared between normal and glaucomatous eyes. Multivariate logistic models were used to assess factors associated with the severity of PLS. Factors considered were age, axial length, glaucomatous damage indices, Bruch membrane opening (BMO) and anterior scleral canal opening parameters, tractional forces (posterior vitreous staging and presence of Bergmeister papilla), circumpapillary choroidal thickness, lamina cribrosa (LC) parameters, and peripapillary scleral (PPS) angle. RESULTS: The frequency of PLS was 70.9% in normal eyes and 72.0% in glaucomatous eyes. There was no difference in frequency and severity between the groups. The presence of Bergmeister papilla was the strongest predictor of a more severe PLS in both normal and glaucomatous eyes (odds ratio [OR] + 9.78, 12.5; both P < .001). A larger PPS angle in normal eyes (OR = 1.19; P = .003) and a larger BMO area and a deeper LC depth in glaucomatous eyes (OR = 1.08, 1.05; both P = .038) were associated with severity of PLS. CONCLUSIONS: The severity of PLS was strongly associated with the presence of Bergmeister papilla, suggesting a traction-related phenomenon. Correlation of PLS severity with larger BMO area and deeper LC depth, which are optic nerve head structures associated with glaucoma, suggested its possible relationship with glaucomatous damage. Evaluation of the intra-optic disc region including the lamina cribrosa (LC) and peripapillary sclera (PPS) is of special interest, because these regions are considered to be the primary site of damage in open-angle glaucoma (OAG).1Quigley 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: 635-649https://doi.org/10.1001/archopht.1981.03930010635009Crossref PubMed Scopus (1053) Google Scholar, 2Miller KM Quigley HA. The clinical appearance of the lamina cribrosa as a function of the extent of glaucomatous optic nerve damage.Ophthalmology. 1988; 95: 135-138https://doi.org/10.1016/s0161-6420(88)33219-7Abstract Full Text PDF PubMed Google Scholar, 3Quigley 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: 673-691https://doi.org/10.1016/0002-9394(83)90389-6Abstract Full Text PDF PubMed Scopus (581) Google Scholar, 4Tezel G Trinkaus K Wax MB Alterations in the morphology of lamina cribrosa pores in glaucomatous eyes.Br J Ophthalmol. 2004; 88: 251-256https://doi.org/10.1136/bjo.2003.019281Crossref PubMed Scopus (57) Google Scholar The advancement of optical coherence tomography (OCT) technology has enabled visualization of microstructures of the optic nerve head (ONH) that are not observed otherwise, providing new insights into ONH structural changes. Recently, a splitting or schisis-like deformation of the prelaminar tissue, prelaminar schisis (PLS), observed on spectral domain OCT (SD-OCT) images, was reported.5Fortune B Pulling and tugging on the retina: mechanical impact of glaucoma beyond the optic nerve head.Invest Ophthalmol Vis Sci. 2019; 60: 26-35https://doi.org/10.1167/iovs.18-25837Crossref PubMed Scopus (29) Google Scholar A higher frequency and a more severe PLS in early glaucomatous eyes in comparison to normal eyes was found in a previous study.6Lowry EA Mansberger SL Gardiner SK et al.Association of optic nerve head prelaminar schisis with glaucoma.Am J Ophthalmol. 2021; 223: 246-258https://doi.org/10.1016/j.ajo.2020.10.021Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar Deeper ONH cupping in normal and mildly glaucomatous eyes6Lowry EA Mansberger SL Gardiner SK et al.Association of optic nerve head prelaminar schisis with glaucoma.Am J Ophthalmol. 2021; 223: 246-258https://doi.org/10.1016/j.ajo.2020.10.021Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar and deeper LC depth (LCD) in advanced glaucomatous eyes7Sung MS Jin HN Park SW Clinical features of advanced glaucoma with optic nerve head prelaminar schisis.Am J Ophthalmol. 2021; 232: 17-29https://doi.org/10.1016/j.ajo.2021.06.007Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar were associated with PLS. These studies implied that mechanical stress accompanying the deepening of ONH cupping may lead to a glial cell–induced disruption in prelaminar connective tissue. However, both studies6Lowry EA Mansberger SL Gardiner SK et al.Association of optic nerve head prelaminar schisis with glaucoma.Am J Ophthalmol. 2021; 223: 246-258https://doi.org/10.1016/j.ajo.2020.10.021Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar,7Sung MS Jin HN Park SW Clinical features of advanced glaucoma with optic nerve head prelaminar schisis.Am J Ophthalmol. 2021; 232: 17-29https://doi.org/10.1016/j.ajo.2021.06.007Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar failed to find a correlation between visual field indices and the presence or severity of PLS, rendering the relationship of PLS and glaucoma to be investigated further. Although deepening of the ONH cup is one possible etiology for tissue disruption in the prelaminar region, the role of posterior vitreous traction and axial length (AXL) also need to be taken into consideration when considering retinal tissue splitting. Sung et al reported an association with shorter AXL and PLS in advanced glaucomatous eyes,7Sung MS Jin HN Park SW Clinical features of advanced glaucoma with optic nerve head prelaminar schisis.Am J Ophthalmol. 2021; 232: 17-29https://doi.org/10.1016/j.ajo.2021.06.007Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar suggesting the possibility of changes in posterior vitreous traction due to AXL-related vitreous liquification to be one factor associated with PLS. Furthermore, peripapillary retinoschisis, which is a similar disruption of the inner retinal layers outside the optic disc, is often associated with longer AXL and glaucoma,8Fortune B Ma KN Gardiner SK Demirel S Mansberger SL Peripapillary retinoschisis in glaucoma: association with progression and oct signs of müller cell involvement.Invest Ophthalmol Vis Sci. 2018; 59: 2818-2827https://doi.org/10.1167/iovs.18-24160Crossref PubMed Scopus (31) Google Scholar, 9Lee EJ Kee HJ Han JC Kee C The progression of peripapillary retinoschisis may indicate the progression of glaucoma.Invest Ophthalmol Vis Sci. 2021; 62: 16https://doi.org/10.1167/iovs.62.2.16Crossref PubMed Google Scholar, 10Ohno-Matsui K Shimada N Yasuzumi K et al.Long-term development of significant visual field defects in highly myopic eyes.Am J Ophthalmol. 2011; 152: 256-265https://doi.org/10.1016/j.ajo.2011.01.052Abstract Full Text Full Text PDF PubMed Scopus (114) Google Scholar and similar associations may exist with intra-disc connective tissue disruptions. The use of swept-source OCT (SS-OCT) enabling better visibility of the vitreo-retinal surface11Lavinsky F Lavinsky D Novel perspectives on swept-source optical coherence tomography.Int J Retina Vitreous. 2016; 2: 25https://doi.org/10.1186/s40942-016-0050-yCrossref PubMed Scopus (67) Google Scholar may provide a deeper understanding of the factors associated with PLS. The purpose of this study is to further elucidate the clinical features of PLS using in normal and glaucomatous eyes possible of ONH changes and tractional including Bergmeister papilla and posterior vitreous into and glaucomatous subjects were using of the of of of and were the of and to the of the of in the study. to and glaucoma were including and of visual with the AXL with and visual field with were the for of this study were as of or AXL and of of OCT and are in one of a the both eyes were the study. of was and in the to angle loss or nerve or retinal myopic eyes or its eyes with optic disc optic posterior of or of glaucoma subjects of or that significant of or significant or = OCT = optical coherence = peripapillary in a new = OCT = optical coherence = peripapillary A normal no including and an open normal optic disc appearance of both eyes on clinical and and normal A glaucomatous an of on the of OCT an open glaucomatous optic disc appearance on clinical and and with to the optic glaucomatous changes. were the Clinical in Google Scholar of OCT and of ONH structures reported et optic nerve head structures associated with axial length in myopic eyes of axial J Ophthalmol. Full Text Full Text PDF PubMed Scopus Google Scholar the ONH and of subjects were a OCT ONH Bruch membrane opening and including both the ONH and were for retinal nerve and circumpapillary choroidal were a The retinal and anterior scleral canal opening were on to BMO the of in to the BMO et optic nerve head structures associated with axial length in myopic eyes of axial J Ophthalmol. Full Text Full Text PDF PubMed Scopus Google Scholar the of of in to the BMO et optic nerve head structures associated with axial length in myopic eyes of axial J Ophthalmol. Full Text Full Text PDF PubMed Scopus Google Scholar and peripapillary were using a the of an on the of the 1988; PubMed Scopus Google Scholar the on and was used for LC B Pulling and tugging on the retina: mechanical impact of glaucoma beyond the optic nerve head.Invest Ophthalmol Vis Sci. 2019; 60: 26-35https://doi.org/10.1167/iovs.18-25837Crossref PubMed Scopus (29) Google et to anterior lamina cribrosa morphology and its in Ophthalmol Vis Sci. PubMed Scopus Google Scholar was as the between the BMO and anterior LC the BMO the inner membrane is often the prelaminar in PLS used of ONH cup depth to assess the relationship between PLS and ONH cup MS Jin HN Park SW Clinical features of advanced glaucoma with optic nerve head prelaminar schisis.Am J Ophthalmol. 2021; 232: 17-29https://doi.org/10.1016/j.ajo.2021.06.007Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar The LC is an with a between and the of the LC anterior PPS angle the of PPS and is as the angle between to the anterior scleral a in the A larger angle a more PPS The were on one was to and was a and and for of the presence and for PLS were on normal and glaucomatous eyes the to of the PLS was as the splitting of prelaminar tissue the BMO of the ONH observed in more of retinal or the prelaminar tissue was on PLS eyes to that the observed was not a between an and the prelaminar tissue. PLS was further into the EA Mansberger SL Gardiner SK et al.Association of optic nerve head prelaminar schisis with glaucoma.Am J Ophthalmol. 2021; 223: 246-258https://doi.org/10.1016/j.ajo.2020.10.021Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar and of retinal into consideration with no PLS. with optical between the of and anterior prelaminar tissue with the with larger more with retinal often the prelaminar tissue. were eyes in the glaucoma with PLS with larger schisis and disruption of the prelaminar tissue, eyes were in in study for Although PLS was on the were on ONH to that the splitting observed in eyes with PLS were not OCT with vitreous visibility the et vitreous in eyes using optical coherence Scopus Google Scholar were used for of with no of the posterior vitreous membrane and with of the posterior vitreous to the papilla and were considered to of et K K vitreous as observed OCT 2018; Full Text Full Text PDF PubMed Scopus Google with and peripapillary with of the posterior vitreous to the papilla and in both the and peripapillary region were considered to of et al with no posterior vitreous membrane the OCT normal eyes and glaucomatous eyes) were to because the and area of were and were the of The presence of Bergmeister papilla was on the ONH as a tissue in the of the ONH into the G et of canal in normal eyes.Am J Ophthalmol. 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Furthermore, indices glaucoma severity as of and were not associated with severity of PLS, suggesting that PLS may not be a These are with an study that reported PLS to be observed more in glaucomatous eyes in normal eyes EA Mansberger SL Gardiner SK et al.Association of optic nerve head prelaminar schisis with glaucoma.Am J Ophthalmol. 2021; 223: 246-258https://doi.org/10.1016/j.ajo.2020.10.021Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar However, the of PLS eyes in the of study to the relationship between glaucomatous damage and splitting of the prelaminar The that the PLS eyes were glaucomatous eyes was in with the previous EA Mansberger SL Gardiner SK et al.Association of optic nerve head prelaminar schisis with glaucoma.Am J Ophthalmol. 2021; 223: 246-258https://doi.org/10.1016/j.ajo.2020.10.021Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar which may that a more severe of PLS is associated with glaucomatous damage. found a higher frequency of PLS in normal eyes in comparison to previous in no difference between the of study. cribrosa morphology has reported to C et in the association of anterior lamina cribrosa depth and glaucoma severity in the and Evaluation Ophthalmol Vis Sci. 2019; 60: PubMed Scopus Google Scholar and the of subjects in study may an impact on may be for this Peripapillary retinoschisis, a similar splitting of the retinal in the peripapillary region, was reported to no impact on visual field EJ of peripapillary retinoschisis on visual field in glaucomatous eyes.Br J Ophthalmol. Scopus Google Scholar its presence or is to be associated with visual field B Ma KN Gardiner SK Demirel S Mansberger SL Peripapillary retinoschisis in glaucoma: association with progression and oct signs of müller cell involvement.Invest Ophthalmol Vis Sci. 2018; 59: 2818-2827https://doi.org/10.1167/iovs.18-24160Crossref PubMed Scopus (31) Google EJ Kee HJ Han JC Kee C The progression of peripapillary retinoschisis may indicate the progression of glaucoma.Invest Ophthalmol Vis Sci. 2021; 62: 16https://doi.org/10.1167/iovs.62.2.16Crossref PubMed Google Scholar may be possible with PLS. studies that PLS may be a the of and intra-disc of the prelaminar tissue as glaucomatous damage and ONH cupping was not with association between visual field indices and the presence of or severity of PLS, be taken into consideration in cross-sectional studies with of glaucomatous Furthermore, the of association of vitreo-retinal traction with the presence of MS Jin HN Park SW Clinical features of advanced glaucoma with optic nerve head prelaminar schisis.Am J Ophthalmol. 2021; 232: 17-29https://doi.org/10.1016/j.ajo.2021.06.007Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar a of the vitreous was not in both studies because of the use of depth which the of the inner retinal layers and vitreous region for better visibility of the deeper ONH depth optical coherence J Ophthalmol. 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Full Text Full Text PDF PubMed Scopus Google Scholar Furthermore, changes with J B et OCT with of retinal 2019; PubMed Google Scholar which for this Although AXL was taken into consideration in may be because the relationship between and AXL is However, as PPS was on a of the of is to be and a comparison of OCT be to the of between PPS and the development of PLS The association of a larger BMO area and a deeper with the severity of PLS in glaucomatous eyes were in with previous EA Mansberger SL Gardiner SK et al.Association of optic nerve head prelaminar schisis with glaucoma.Am J Ophthalmol. 2021; 223: 246-258https://doi.org/10.1016/j.ajo.2020.10.021Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar,7Sung MS Jin HN Park SW Clinical features of advanced glaucoma with optic nerve head prelaminar schisis.Am J Ophthalmol. 2021; 232: 17-29https://doi.org/10.1016/j.ajo.2021.06.007Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar with the that larger PPS et sclera a that is more in glaucoma eyes.Br J Ophthalmol. 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PubMed Scopus Google Scholar as as an association with shorter AXL and PLS in advanced glaucomatous eyes,7Sung MS Jin HN Park SW Clinical features of advanced glaucoma with optic nerve head prelaminar schisis.Am J Ophthalmol. 2021; 232: 17-29https://doi.org/10.1016/j.ajo.2021.06.007Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar suggesting relationship between AXL and PLS. Although the relationship between AXL and PLS is because the frequency of PLS was not compared to myopic eyes in the previous is a possibility that the of study myopic eyes However, to be an myopic AXL study on the of PLS in myopic normal and glaucoma which is of because the of eyes into this for the association between AXL and PLS is that posterior vitreous traction may be the of optic disc cupping in eyes with longer AXL due to early of the posterior However, AXL was not as an factor for the severity of PLS in both the normal and glaucomatous eyes of Furthermore, the that staging was not the for PLS in of that AXL was not associated with a more severe PLS. However, an association with shorter AXL and Bergmeister papilla has reported in J K The and of papilla in myopic are associated with axial Vis 2021; Scopus Google Scholar and be a possible relationship the presence of Bergmeister papilla, and PLS. There are that may the of study. 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