Thickness of the lamina cribrosa and peripapillary sclera in Rhesus monkeys with nonglaucomatous or glaucomatous optic neuropathy
2011; Wiley; Volume: 89; Issue: 5 Linguagem: Inglês
10.1111/j.1755-3768.2011.02121.x
ISSN1755-3768
AutoresJost B. Jonas, Sohan Singh Hayreh, Yong Tao,
Tópico(s)Corneal surgery and disorders
ResumoActa OphthalmologicaVolume 89, Issue 5 p. e423-e427 Free Access Thickness of the lamina cribrosa and peripapillary sclera in Rhesus monkeys with nonglaucomatous or glaucomatous optic neuropathy Jost B. Jonas, Jost B. Jonas Department of Ophthalmology, Medical Faculty Mannheim of the Ruprecht-Karls-University Heidelberg, Mannheim, GermanySearch for more papers by this authorSohan S. Hayreh, Sohan S. Hayreh Departments of Ophthalmology and Visual Sciences, College of Medicine, University of Iowa, Iowa City, IA, USASearch for more papers by this authorTao Yong, Tao Yong Department of Ophthalmology, Medical Faculty Mannheim of the Ruprecht-Karls-University Heidelberg, Mannheim, GermanySearch for more papers by this author Jost B. Jonas, Jost B. Jonas Department of Ophthalmology, Medical Faculty Mannheim of the Ruprecht-Karls-University Heidelberg, Mannheim, GermanySearch for more papers by this authorSohan S. Hayreh, Sohan S. Hayreh Departments of Ophthalmology and Visual Sciences, College of Medicine, University of Iowa, Iowa City, IA, USASearch for more papers by this authorTao Yong, Tao Yong Department of Ophthalmology, Medical Faculty Mannheim of the Ruprecht-Karls-University Heidelberg, Mannheim, GermanySearch for more papers by this author First published: 18 February 2011 https://doi.org/10.1111/j.1755-3768.2011.02121.xCitations: 9 Dr J. JonasUniversitäts-AugenklinikTheodor-Kutzer-Ufer 1-368167 MannheimGermanyTel: + 49 621 383 2242Fax: + 49 621 383 3803Email: Jost.Jonas@augen.ma.uni-heidelberg.de AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Abstract. Purpose: To measure the thickness of the lamina cribrosa and peripapillary sclera in monkeys with a nonglaucomatous optic nerve damage and to compare that with those of monkeys with glaucomatous optic neuropathy. Methods: The study included 22 monkey eyes (Macaca mulatta) which had undergone a temporary experimental central retinal artery occlusion (CRAO) and seven monkey eyes in which experimental glaucoma was unilaterally produced. We measured histomorphometrically the thickness of the lamina cribrosa and peripapillary sclera. Results: The lamina cribrosa was significantly thicker in the CRAO group than in the glaucoma group (central region: 212 ± 46 μm versus 167 ± 17 μm; p = 0.009). The thickness of the peripapillary sclera at the optic disc border (253 ± 39 μm versus 192 ± 21 μm; p = 0.001) and outside of the optic nerve meninges (408 ± 70 μm versus 314 ± 64 μm; p = 0.006) was significantly greater in the CRAO group. Conclusions: In monkey eyes with a temporary CRAO as a model for nonglaucomatous optic nerve damage, the lamina cribrosa is significantly thicker than in monkey eyes with experimental glaucomatous optic nerve damage. It may suggest that the loss of optic nerve fibres might not be the reason for the thinning of the lamina cribrosa in eyes with advanced glaucoma. The thinner peripapillary sclera in the glaucomatous eyes may suggest that the monkey sclera is more vulnerable to stretching with increased intraocular pressure than the human eye for which no glaucoma-related lengthening of the eyeball and thinning of the peripapillary sclera have been observed. Introduction Recent studies on the biomechanics and histomorphometry of the optic nerve head have shown that the architecture of the lamina cribrosa in association with its anchoring in the peripapillary sclera may play a role in the physiology and pathophysiology of the optic nerve head, particularly for the pathogenesis of glaucomatous optic neuropathy (Bellezza et al. 2000, 2003; Burgoyne & Morrison 2001; Downs et al. 2001, 2007; Sigal et al. 2004, 2005, 2007; Burgoyne et al. 2005). Investigations also revealed that in end stage of glaucoma, the lamina cribrosa becomes markedly thinned and stretched backward (Jonas et al. 2003). The mechanism of this thinning of the lamina cribrosa in advanced glaucomatous optic neuropathy has remained debatable so far. It was, therefore, the purpose of our study to compare by histomorphometry the thickness of the lamina cribrosa and of the peripapillary sclera in eyes with glaucomatous and nonglaucomatous optic nerve damage in a rhesus monkey model. We examined monkey eyes in our study: (i) after an experimental transient occlusion of the central retinal artery (CRAO) as model of nonglaucomatous optic nerve damage and (ii) with experimental glaucoma. Methods The study included monkey (Macaca mulatta) eyes which, at Iowa City, USA, had a temporary experimental CRAO (Hayreh & Weingeist 1980; Hayreh & Jonas 2000) or production of unilateral experimental glaucoma (Hayreh et al. 1998), and for which histological sections through the optic nerve head were available. Unilateral experimental glaucoma was produced by multiple applications of argon laser to the trabecular meshwork (Hayreh et al. 1998). Temporary CRAO was produced by transient clamping of the central retinal artery at its site of entry into the dural sheath of the optic nerve (Hayreh & Weingeist 1980; Hayreh & Jonas 2000). In addition, atherosclerosis and experimental arterial hypertension had been produced in some monkeys. The methods of producing experimental glaucoma or CRAO and systemic arterial hypertension and atherosclerosis were described in detail previously (Hayreh & Weingeist 1980; Hayreh et al. 1998; Hayreh & Jonas 2000). The contralateral eyes were not available for this study because they had already been used for other earlier studies (May et al. 1997; Hayreh et al. 1999). The study design complied with the National Institute of Health’s as well as University of Iowa’s Institutional Guidelines for the Care and Use of Laboratory Animals. All animals were serially examined under ketamine anaesthesia (8–10 mg/kg body weight), before and during follow-up of the induction of CRAO or glaucoma. These examinations included intraocular pressure measurement by Goldmann applanation tonometry, ophthalmoscopic examination and colour fundus photography. Before sacrificing, photographs of the fundus were taken in all animals. The enucleated globes were immediately placed in 4% buffered formalin. They were fixed for no less than 72 hr, following which they were opened in a standard horizontal pupil-optic nerve plane, thereby incorporating the macular region, along with the optic nerve. The preparation of the globes was identical for both study groups. The globes were prepared in routine manner for light microscopy. The cut anterior–posterior segments of the globe, going through the pupil and the optic nerve, were dehydrated in alcohol, imbedded in paraffin, sectioned for light microscopy and stained by the periodic acid-Schiff (PAS) method. For all eyes, one section running through the central part of the optic disc was selected for further evaluation. The histological slides were digitized and morphometrically analysed using a microscope with built-in software for planimetric measurements (LEICA IM50 1.20, Leica Microsystems AG, Switzerland). We measured the thickness of the lamina cribrosa in the central, midperipheral and peripheral regions and determined thickness of the sclera at the optic disc border and just outside the dural sheath of the optic nerve (Fig. 1). A similar method was recently applied on human globes (Ren et al. 2009). Figure 1Open in figure viewerPowerPoint Microphotograph of a monkey optic nerve head showing the measurement points of the sclera at the optic disc border (‘A’) and just outside the optic nerve meninges (‘B’). Bar: 250 μm. Statistical analysis was performed by using a commercially available statistical software package (SPSS for Windows, version 17.0; SPSS, Chicago, IL, USA). The data were presented as means and standard deviations as well as medians and ranges. For the comparison of the study groups, the nonparametrical statistical tests of Mann–Whitney test for unpaired samples were applied. The level of statistical significance was 0.05 in all tests. Results The study included 22 monkey eyes (22 monkeys) in the CRAO group and seven monkey eyes in the glaucoma group. The mean age of the monkeys was 18 ± 3 years (range: 13–22 years). Temporary CRAO had been produced by the transient clamping of the central retinal artery for a period of 127 ± 28 min (range: 97–165 min). In addition, atherosclerosis had been produced in 6 monkeys, experimental arterial hypertension in four monkeys, and both atherosclerosis and arterial hypertension in 11 monkeys. In the glaucoma group, the duration of elevated intraocular pressure glaucoma was 21 ± 15 months (range: 7–40 months). During the follow-up period, the frequency of intraocular pressure measurements depended upon the level of intraocular pressure in each eye; the higher the intraocular pressure, the more frequently it was measured, i.e. 2–3 times a week when the intraocular pressure was >60 mm Hg, weekly for intraocular pressure in the forties or fifties and monthly for intraocular pressures of <40 mm Hg. Our objective was to maintain an intraocular pressure between 30 and 40 mm Hg to mimic the clinical situation of moderate ocular hypertension. Because, with the argon laser trabecular application, it is impossible to achieve a desired level of intraocular pressure on a long-term basis, the intraocular pressure often tended to go higher than the desired levels if left alone. Therefore, to maintain our desired level of intraocular pressure (i.e. 30–40 mmHg), we had to use ocular hypotensive drops, such as topical betabockers and miotics, in 90% of the glaucoma eyes. The intraocular pressure in the monkeys of the CRAO group was in the normal range, and an anti-glaucomatous medication was not given to any monkey of this group. Upon assessments of the fundus photographs, the glaucomatous eyes showed marked glaucomatous optic nerve damage in the sense of a pronounced loss of neuroretinal rim when compared to the photographs taken at baseline of the study (Hayreh et al.1998). The eyes of the CRAO showed a loss in the retinal nerve fibre layer and pallor of the neuroretinal rim when compared to the baseline photographs. The size and shape of the rim did not differ from the baseline examination (Hayreh & Jonas 2000). The contralateral eyes of the monkeys were not available for this study because they had already been used for other earlier studies applying techniques that made an assessment for the purpose of this study impossible. The mean thickness of the lamina cribrosa in the central region was significantly thicker in the CRAO group than in the glaucoma group (212 ± 46 μm versus 167 ± 17 μm; p = 0.009) (Fig. 2). In the intermediate region and the peripheral region of the optic nerve head, respectively, the lamina cribrosa was thicker, however, not significantly in the CRAO group than in the glaucoma group (209 ± 50 μm versus 181 ± 17 μm (p = 0.11) and (235 ± 47 μm versus 203 ± 21 μm (p = 0.07). Figure 2Open in figure viewerPowerPoint Boxplot showing the statistically significant (p = 0.009) difference in the mean thickness of the central lamina cribrosa between 22 rhesus monkeys after an experimental occlusion of the central retinal artery and seven monkeys with experimental glaucoma. The shortest distance between the retrobulbar cerebrospinal fluid space and the intraocular space (defined as surface of the retinal nerve fibre layer or surface of the optic nerve head) was significantly longer in the CRAO group than in the glaucoma group (828 ± 136 μm versus 494 ± 49 μm; p < 0.001). The thickness of the sclera at the optic disc border (253 ± 39 μm versus 192 ± 21 μm; p = 0.001) (Fig. 3) and at the outer margin of the dural sheath of the optic nerve (408 ± 70 μm versus 314 ± 64 μm; p = 0.006) (Fig. 4) was significantly greater in the CRAO group than in the glaucoma group. Figure 3Open in figure viewerPowerPoint Boxplot showing the statistically significant (p = 0.001) difference in the thickness of the sclera at the optic disc border (253 ± 39 μm versus 192 ± 21 μm) between 22 rhesus monkeys after an experimental occlusion of the central retinal artery and seven monkeys with experimental glaucoma. Figure 4Open in figure viewerPowerPoint Boxplot showing the statistically significant (p = 0.006) difference in the thickness of the sclera at the outer margin of the dural sheath of the optic nerve (408 ± 70 μm versus 314 ± 64 μm) between 22 rhesus monkeys after an experimental occlusion of the central retinal artery and seven monkeys with experimental glaucoma. Based on the significant difference in the lamina cribrosa thickness between the CRAO group and the glaucoma group, we then performed a multivariate linear regression analysis, with central thickness of the lamina cribrosa as dependent variable, study group (CRAO versus glaucoma) as independent variable and the presence of atherosclerosis, hypertension or both as additional independent variables. It revealed that the central lamina cribrosa thickness was significantly associated with the study group (p = 0.025; standardized coefficient beta: −0.44; regression coefficient: −48; 95% confidence interval: −90, −7), while the association with atherosclerosis and arterial hypertension was not significant (p = 0.52). In a similar manner, the scleral thickness at the optic disc border and at the outer margin of the dural sheath of the optic nerve, respectively, was significantly associated with the CRAO group (p = 0.001 (standardized coefficient beta: −0.44; regression coefficient: −67; 95% confidence interval: −102, −31) and p = 0.002 (standardized coefficient beta: −0.57; regression coefficient: −110; 95% confidence interval: −177, −43), resp.), and they were not significantly associated with the presence of atherosclerosis, hypertension or both (p = 0.42, and p = 0.64). Discussion Glaucomatous optic neuropathy and nonglaucomatous optic nerve damage have in common a loss of retinal nerve fibre layer and a decrease in the retinal artery diameter. Glaucomatous optic neuropathy in contrast to nonglaucomatous optic nerve damage shows a development of parapapillary atrophy and optic disc haemorrhages, loss of neuroretinal rim and enlargement and deepening of the optic cup (Hayreh 1974; Jonas et al. 1991, 2000; Jonas & Schiro 1994; Jonas & Xu 1994; Hayreh & Jonas 2001). It was unclear whether the histology of the lamina cribrosa differs between eyes with glaucomatous optic neuropathy and eyes with nonglaucomatous optic nerve atrophy, because clinical studies on the morphology of the optic nerve head have been unable to measure the thickness or other parameters of the lamina cribrosa. The results of our study suggest that the lamina cribrosa in monkey eyes with a transient occlusion of the central retinal artery as a model for nonglaucomatous optic nerve damage was significantly thicker than in monkey eyes with experimental glaucomatous optic nerve damage. Additionally, the results showed that the peripapillary sclera was significantly thinner in the glaucomatous monkey eyes than in the monkey eyes after CRAO. Because the loss of optic nerve fibres is one of the main factors that glaucomatous optic neuropathy and nonglaucomatous optic nerve damage have in common, one may postulate that the finding of a thinner lamina cribrosa in the glaucoma group cannot be caused by the loss of optic nerve fibres (which is present in both types of atrophy) but that an additional factor may be present in glaucoma. It may suggest that the loss of optic nerve fibres is not the primary reason for the thinning of the lamina cribrosa in eyes with advanced glaucoma (Hayreh et al. 1998). Previous studies have also addressed glaucoma-related changes in the lamina cribrosa of monkeys with experimentally elevated intraocular pressure. In a recent investigation (Yang et al. 2007), Yang and colleagues examined serial sections of the optic nerve head and the peripapillary sclera from both eyes of three monkeys with unilateral early glaucoma and created three-dimensional reconstructions. They found that the thickness of the lamina cribrosa varied substantially between the three normal monkey eyes and that the lamina cribrosa was profoundly thicker within the three eyes with early glaucoma than in the normal eyes. Additionally, the lamina cribrosa was posteriorly deformed in the early glaucomatous eyes with marked differences in the magnitude between the eyes (Yang et al. 2007). The discrepancy between the results of Yang and colleagues and ours may be because of differences in the stage of the disease, with Yang′s study including monkey eyes with early glaucoma and our study including monkey eyes with advanced glaucomatous optic neuropathy. The peripapillary sclera was significantly thinner in the glaucomatous monkey eyes than in the monkey eyes after CRAO. Previous studies in adult monkeys with unilateral glaucoma showed a lengthening of the glaucomatous eyes compared to the fellow control eyes (Hayreh et al. 1998; Yang et al. 2007). It may suggest that the monkey sclera is vulnerable to stretching with increased intraocular pressure. That seems to be the only plausible explanation for the scleral thinning in the peripapillary region as observed in our study, as well as the scleral thinning at other places of the monkey eye as reported by Downs and colleagues (2001). Because no glaucoma-related lengthening of the eyeball and thinning of the peripapillary sclera have been observed in adult human glaucomatous globes, it may make one wonder whether the monkey glaucoma model differs in some aspects from glaucoma in humans. That may also have implications for the changes seen in the lamina cribrosa in monkeys versus those in humans. It can be argued that our study had the following limitations. First, generally there was some interindividual variability in the measurements of the lamina cribrosa and the thickness of the peripapillary sclera (2-4). This interindividual variability was partially because of limitations of the study techniques such as oblique histological sectioning and variations in the locations from which the sections were taken. The interindividual variability in the measurements led to a marked overlapping between the study groups (2-4). Second, there was no control group without any optic nerve damage. Without normal, untreated control eyes, however, it may be difficult to know what was treatment effect and what was physiologic variability. The conclusions of the study can, therefore, only refer to the comparison of eyes after an experimental temporary CRAO and eyes with experimental glaucoma. In view of the inter-eye variability in the thickness measurements of the lamina cribrosa as also reported by Yang and colleagues (2007), one may also argue that without laminar thickness measures for contralateral normal control eyes, it may have been difficult to know whether the CRAO animals truly had a thicker lamina when compared to the glaucoma animals, or whether the CRAO animals simply happened to have thicker laminas to start. The same issue may be discussed for the scleral thickness measurements. Third, we measured only one section per eye and this was not consistent among and between groups. Serial sections of the globes were not available so that it was not possible to determine whether the histological sections located in the very centre of the optic disc or paracentrally would have provided different findings. Because there were no marked differences in the thinning of the lamina cribrosa between the central region versus the peripheral region of the optic disc, the inaccuracy in the exact localization of the histological section might not have markedly influenced the determinations of the lamina cribrosa thickness and the conclusions of the study. In addition, this limitation in the design of the study again held true for both study groups so that this systemic error might not have markedly influenced the results of the comparison of the study groups. Fourth, the eyes examined in our study were fixed at an intraocular pressure of about zero mm Hg. It rendered reliable determinations of the position of the lamina cribrosa impossible. Previous studies on nonhuman primates by Burgoyne and colleagues have shown differences in the laminar and peripapillary scleral morphology between eyes fixed at physiologic pressures and at zero mm Hg (Yang et al. 2007). It could be argued that it might have introduced an artefact in our study. The significant difference in thickness of the peripapillary sclera at the optic disc border (p = 0.001) and outside of the optic nerve meninges (p = 0.006) between the two groups cannot been explained by fixation of the eyes at zero intraocular pressure. Fifth, all the eyes in our study were fixed immediately on enucleation; therefore, the possibility of post-mortem swelling of the tissue after enucleation and because of the histological preparation cannot explain the differences between the two groups. Sixth, the number of glaucomatous monkey eyes included into the study was too small for a statistical analysis of a potential association between the thinning of the lamina cribrosa and the duration of intraocular pressure elevation, the level of intraocular pressure or the stage of the disease. In conclusion, the present study suggests that in monkey eyes with a temporary CRAO as a model for nonglaucomatous optic nerve damage, the lamina cribrosa is significantly thicker than in monkey eyes with experimental glaucomatous optic nerve damage. Future studies may address the reasons for this difference between the two groups. The thinner peripapillary sclera in the glaucomatous eyes may suggest that the monkey sclera is more vulnerable to stretching with increased intraocular pressure than the human eye for which no glaucoma-related lengthening of the eyeball and thinning of the peripapillary sclera have been observed. Acknowledgements Supported by Dr S. S. Hayreh’s grant EY-1576 from the U.S. National Institutes of Health and in part by unrestricted grants from Research to Prevent Blindness, Inc., New York, USA. Proprietary interest: none. References Bellezza AJ, Hart RT & Burgoyne CF (2000): The optic nerve head as a biomechanical structure: initial finite element modeling. 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