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Show Optical Coherence Tomography Shape Analysis of the Peripapillary Retinal Pigment Epithelium Layer in Presumed Optic Nerve Sheath Meningiomas Patrick Sibony, MD, Matthew Strachovsky, MD, Robert Honkanen, MD, Mark J. Kupersmith, MD Background: Geometric morphometrics (GM) was used to compare the shape of the peripapillary retinal pigment epithelium-Bruch's membrane (ppRPE) layer imaged on spectral domain optical coherence tomography (SD-OCT) of patients with presumed optic nerve sheath meningiomas (pONSM) and normal subjects. Methods: We compared 2 groups: 30 normals to 10 patients (11 eyes) with pONSM. We digitized 20 equidistant semi-landmarks on OCT images of the ppRPE-layer, span-ning 2500 mm on each side of the neural canal opening (NCO). Data were analyzed using standard GM techniques including a generalized least squares Procrustes superim-position, principal component analysis (PCA), thin-plate spline, and permutation statistical analysis to evaluate dif-ferences in shape. We also analyzed other variables with respect to shape including tumor size-proximity to the globe, age, retinal nerve fiber layer, and optic disc height. Results: All pONSM patients were female (age 37-66 years); 10 had unilateral and 1 had bilateral optic nerve involvement. Ten of the eyes had optic disc edema at pre-sentation, 4 went on to develop shunt vessels, and 4 had optic atrophy. The ppRPE-layer bordering the NCO in nor-mals is V-shaped pointing away from the vitreous; the ppRPE-layer in pONSM is indented causing an inverted-U shaped deformation skewed nasally toward the vitreous. PCA showed a significant difference between normals and pONSM (permutation, n = 10,000, P = 0.001). The size and proximity of the tumor to the globe correlates with the shape of the ppRPE-layer (r = 0.75, P = 0.04). Correlation between shape variables and RNFL thickening (r = 0.51), optic disc height (r = 0.67), and age (r = 0.67) were not statistically significant. Conclusion: The shape of the RPE layer in pONSM is characterized by an inverted-U shape or indentation that differs significantly from normals. It is indistinguishable from the shape we previously reported in papilledema and is not caused by disc edema. The mechanism in pONSM is unknown but may involve a change in the compliance of the nerve and/or localized sequestration of cerebrospinal fluid in the distal optic nerve sheath. Journal of Neuro-Ophthalmology 2014;34:130-136 doi: 10.1097/WNO.0000000000000107 © 2014 by North American Neuro-Ophthalmology Society Spectral domain optical coherence tomography (SD-OCT) is a useful way of imaging the surface of the optic disc and peripapillary retina in a variety of optic neuropathies. For example, the average thickness of the retinal nerve fiber can be used to assess the degree of optic disc edema (1-5). The SD-OCT can also image subsurface structures such as the peripapillary retinal pigment epithelium-Bruch's mem-brane (ppRPE) layer and choroid. Histomorphometric stud-ies and in vivo imaging in animals and humans have shown that a chronic increase in the intraocular pressure can poste-riorly displace the peripapillary sclera and lamina cribosa (6-13). Conversely, increased intracranial pressure can deform the sclera and ppRPE-layer anteriorly toward the vitreous (14,15). In extending this line of study, we analyzed the shape of the ppRPE-layer in patients with presumed meningiomas of the optical nerve sheath (pONSM) to char-acterize the shape deformation and identify tumor-related factors that might affect this deformation. METHODS We used geometric morphometrics (GM) to quantitatively analyze the shape of the ppRPE-layer imaged on the Department of Ophthalmology (PS, MS, RH), SUNY Eye Institute, State University New York at Stony Brook, UHMC, Stony Brook, New York; and INN at Roosevelt Hospital and New York Eye and Department of Neuro-ophthalmology, Ear Infirmary (MJK), New York, New York. The authors report no conflicts of interest. Supported in part by National Eye Institute Grants U10 EY017281- 01A1 and U10 EY017281-01A1S1 and departmental educational research grant from Davis Optical. Address correspondence to Patrick Sibony, MD, Department of Ophthalmology, University Hospital and Medical Center, Health Sciences Center, SUNY Stony Brook, Stony Brook, NY 11794; E-mail: patrick.sibony@stonybrook.edu 130 Sibony et al: J Neuro-Ophthalmol 2014; 34: 130-136 Original Contribution Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. SD-OCT raster. GM defines shape as the geometric property of a form that remains after filtering out variations in position, scale, and orientation. It is a well-established technique developed to quantify and statistically analyze variation in the shape of biological forms and their covariation with other variables using conventional multivar-iate statistical methods (16-19). It has been extensively used in the fields of biology, anthropology, and paleontology. The analytic techniques used in GM are complex but accessible using a variety of software applications that are widely available. For those readers who wish to learn more, Sanfilippo et al (18,20) provide an overview of shape anal-ysis that includes a discussion of GM and its application in assessing the shape of the optic cup in glaucoma. More detailed information can be found in the monograph by Zelditch et al (16) and a Web site published elsewhere (15) and described below. This study was approved by the SUNY Stony Brook Committee on Research Involving Human Subjects. Patients We analyzed 11 eyes from 10 patients with a diagnosis of pONSM. The presumptive diagnosis was based on both clinical and magnetic resonance imaging (MRI) findings, which consisted of unilateral (9 cases) or bilateral (1 case) slowly progressive vision loss, signs of optic neuropathy (with optic disc edema or optic atrophy), and enlargement and enhancement of the prechiasmal optic nerve sheath on magnetic resonance imaging. None of the cases were confirmed pathologically. The demographics and key clinical findings are summarized in Figure 1. We compared these patients to 30 normal eyes. Among normals, we excluded any patients with abnormal acuity, color vision, a relative afferent pupillary defect, elevated intraocular pressure; abnor-mal visual fields, ophthalmoscopic findings or SD-OCT evi-dence of an optic neuropathy, optic atrophy, glaucoma, or congenital disc anomalies (e.g., drusen, hypoplasia, oblique insertion, tilting, high myopia, staphylomas, or otherwise dysplastic). Image Acquisition SD-OCT were acquired with a Cirrus SD-OCT (Carl Zeiss Meditec, Inc, Dublin, CA). Sharply focused uniformly illuminated images centered over the optic nerve head were obtained using 2 standard protocols: (1) optic disc cube 200 · 200 and (2) a 5-line horizontal high definition raster (9 mm long, 0.25 mm intervals). The raster scan was posi-tioned through the central portion of the optic disc with signal strength of $7. Images were saved in the highest quality .jpeg format. To more accurately assess the image (shape), we converted the display aspect ratio from 3:2 (750 · 500 pixels) (Fig. 2A, C) to a true aspect ratio of 9:2 (750 · 167 pixels) (Fig. 2B, D), which has a uniform spatial scale along both vertical and horizontal dimensions. Digitizing Structural Semi-landmarks Imaging software (Photoshop; Adobe Systems, San Jose, CA) was used to superimpose a transparent line grid spanning 2500 mm on either side of the neural canal open-ing (NCO). The grid was positioned parallel to the flattest portion of the ppRPE-layer on both sides of the NCO, with a starting reference point positioned at the innermost ter-mination of the ppRPE-layer. The grid was used to position 10 semi-landmarks (slightly less than 278 mm apart) along the posterior border of the ppRPE-layer on the temporal and nasal side of the NCO. Points 1 to 10 were placed temporally and 11 to 20 nasally. Left eye images were flip-ped horizontally so that all shape figures depict the nasal RPE on the right side of the image; the temporal RPE is located on the left side (Fig. 2B). Geometric Morphometric Analysis We used GM tps software (19) to analyze the digitized semi-landmarks for each subject including tpsUtil, tpsDig2, FIG. 1. Summary of age, gender, laterality, location, and relative size of the tumor along the optic nerve in 10 patients, 11 eyes. Spectral domain optical coherence tomography images are displayed using the 3:2 aspect ratio for both the affected and unaffected eye for comparison. One patient had bilateral optic nerve involvement (eyes 7 and 8). The images are arranged in relative order with respect to shape. Cases 1-5 show decreasing degrees of inverted U-shapes, whereas the deformation in cases 6-10 consists of a relative flattening when compared with the normal side. Note the shape of the peripapillary retinal pigment epithelium-Bruch's membrane in patient number 9, with the smallest most remote tumor, showed little deformation compared with the normal eye. OD, right eye; OS, left eye. Sibony et al: J Neuro-Ophthalmol 2014; 34: 130-136 131 Original Contribution Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. tpsRegr, and tpsPLS. The software performs a generalized least squares Procrustes superimposition which normalizes the shapes by filtering out differences in location, size, and rotation; a thin-plate spline that uses an algorithm to depict shape differences as a smooth deformation of one shape into another and generates shape variables that can be analyzed with conventional multivariate statistical methods; and principal component analysis (PCA) to identify and display the main sources of shape variance between subjects. Generalized Least Squares Procrustes Superimposition Generalized least squares Procrustes superimposition is the iterative process of estimating a mean shape and then superimposing all of the objects onto this mean shape. This is performed in 3 steps (16). First, the set of points for each subject is adjusted so that their centroid (mean of all of the x coordinates, mean of all the y coordinates) is translated to the origin. This is done by subtracting centroid coordinates from the coordinates of each landmark. Second, each config-uration is scaled by dividing by the centroid size (the square root of the summed squared distances of each landmark from the centroid of its landmark configuration). Third, rotational differences are removed by iteratively minimizing the summed squared distances between corresponding landmarks. Thin-Plate Spline The thin-plate spline has 2 important functions. First, it is used to depict shape differences as a smooth deformation of one shape into another using an algorithm that interpolates potential changes between landmarks of a reference shape (the mean shape) and the shape it is being compared with. These same shape differences can also be visualized using vectors at each landmark showing the magnitude and direction of the differences at each landmark. The thin-plate spline is also used to define a set of shape variables, partial warps, that capture the shape differences among the objects being compared. The partial warp scores provide data matrices that can be analyzed with conven-tional multivariate statistical methods. Principal Component Analysis Because shape variation is multidimensional, PCA was used to express as much of the variation as possible in just a few dimensions that are linear combinations of the partial warps. This allows one to identify and display most of the variation in shape between subjects. The relative contribu-tion of each dimension is proportional to its variance. The tpsRelW software was used for these computations. Statistical Analysis A test statistic adapted to assessing shape differences was proposed by Goodall (16,21). It compares sums of squared Procrustes differences between and within the samples being compared and expresses it as an F-ratio. Valid statis-tical tests can be made by comparing the observed F value to an empirical distribution based on a large number (10,000 FIG. 2. Spectral domain optical coherence tomography (SD-OCT) 9 mm-raster comparing a normal eye from signature case 1 with a presumed optic nerve sheath meningioma illustrating the corrections for aspect ratio, semi-landmark placement and an example of the inverted-U shape and V-shape referred to in the text. A. Normal subject SD-OCT raster scan using the standard jpg image output (9 mm; aspect ratio of 3:2; 750 · 500 pixels). Note that the verti-cal (300 mm) and horizontal (900 mm) box scale differ, resulting in a 3-fold vertically stretched image. This image demonstrates the V-shape of the retinal pigment epithelium- Bruch's membrane (RPE) layer that gently slopes away from the vitreous typically seen in normal subjects. B. Corrected 9-mm image that eliminates vertical stretch by adjusting the vertical scale to reflect the actual shape of the peripapillary eye wall. The image correction, used in our analysis of shape, has an aspect ratio of 9:2 (750 · 167 pixels). The numbered points demonstrate the placement of 10 equidistant semi-landmarks that define the shape of the RPE (starting at the border of the NCO) and spanning 2500 mm on the nasal and temporal side of the neural canal. C. Signature case 1 of a patient with a presumed optic nerve sheath meningioma (9 mm, 3:2 aspect ratio; 750 · 500 pixels). The yellow arrows outline the inverted U-shape deformation, in this case severely indenting the globe toward the vitreous. D. The same case 1 after image correction (9 mm, aspect ratio to 9:2, 750 · 167 pixels). 132 Sibony et al: J Neuro-Ophthalmol 2014; 34: 130-136 Original Contribution Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. in this study) of random permutations of the assignments of individuals to the groups being compared. The proportion of Goodall's F statistics from permuted data sets that are equal to or larger than the observed Goodall's statistic is interpreted as the probability value for the test. Goodall's F test only considers the total amount of shape variation and does not display the nature of the differences. For traditional morphometric measurements, for exam-ple, disc elevation, average RNFL, and NCO diameters, we used Student t test and analysis of variance where appropri-ate. We analyzed how shape variables might covary with a variety of factors including age, refractive error, RNFL thickness, elevation of the optic disc, overall length of the tumor (size), and its proximity to the globe. Correlation between shape variables and RNFL, disc height, age, and tumor size and proximity to the globe were assessed using a Partial least squares analysis (using J Rohlf's tpsPLS soft-ware). MRI was used to measure the (1) length of the tumor and (2) proximity to the globe (measured as the distal lead-ing edge of tumor to the posterior wall of the globe in millimeters). We also used an algorithm that combined the length of the tumor with a weighted score that was based on its proximity to the globe. For example, tumors ,2 mm from the globe received 20 points in addition to the length of the tumor, ,5 mm received 10 additional points, ,10 mm received 5 additional points, and so on. RESULTS Ten women with presumed ONSM between the ages of 37-66 years (mean, 48.7 years) were followed over an aver-age of 58 months (range, 32-141 months). Nine of the patients had a unilateral lesion, 1 patient had bilateral involvement, with 7 right eyes and 3 left eyes (Fig. 1). At presentation, 10 of the eyes had optic disc edema, 1 had optic atrophy. Four of the eyes went on to develop optic atrophy. Four went on to develop retinochoroidal venous collaterals (optociliary shunt vessels). The pONSM of 2 patients showed calcification on computed tomography (CT). The MRI in all cases showed thickening or enlarge-ment of the optic nerve with enhancement, usually along the optic nerve sheath. The greatest deformation was associ-ated with meningiomas abutting the globe, although shape deformation was also observed among patients with tumors remote from the globe. There was one exception with a nor-mal shape in a patient where the tumor was distant from the globe located at the orbital apex and optic canal. OCT data at presentation were not available in 4 of the cases. However, after a mean follow-up of 58 months, data from the most recent visit showed that the mean RNFL thickness was distributed bimodally. Those with chronic disc edema averaged 156 mm (±44 mm), and those with optic atrophy averaged 67.4 mm (±6.5 mm). The unaffected eye averaged 92.6 mm (±8.9 mm) compared with normal subjects with a mean of 92.2 mm (±9.6 mm). A generalized Procrustes superimposition of 20 semi-landmarks for 41 patients (30 normal optic discs and 11 pONSM eyes) is shown in the scatter plot (Fig. 3A). The consensus or mean shapes of the Procrustes transformed semi-landmarks for each group are shown in Figure 3B demonstrating the differences in the shape of the ppRPE-layer in normals vs pONSM. Note that these shapes were obtained from images with an aspect ratio 9:2. However, the horizontal raster images shown in Figure 1 are displayed as they are generated by the Cirrus SD-OCT with a 3:2 aspect ratio. Our results demonstrate that the mean ppRPE-layer in normals has a V-shaped configuration sloped outwardly (away from the vitreous) as it approaches its central margin at the NCO. In contrast, the consensus (mean) shape for subjects with pONSM have an inverted-U shaped ppRPE-layer that is anteriorly displaced toward the vitreous. There is slight nasal skew in the inverted-U shape compared with the relatively symmetrical V-shape in normals. The differ-ence between the 2 groups was highly significant at P = 0.001 (permutation statistics). Two examples of a normal V-shaped RPE layer and an inverted U-shape RPE layer are illustrated both in the uncorrected (3:2 aspect ratio) and corrected (9:2 aspect ratio) forms in Figure 2. Figure 1 displays each of the uncorrected raster scans (3:2 aspect ratio) from both the affected and the contralateral unaf-fected eye for comparison. The deformations vary from an obvious inverted U-shape indentation of the globe (e.g., 1-5) to mild relative flattening of the globe compared with the normal side (e.g., 6-10). There is no apparent deformation in patient 11 who had the smallest tumor furthest from the globe. A variance-covariance matrix of the shape variables derived from both groups of patients was used to perform a PCA (using tpsRelW software (19)). The first 2 principal components together account for 81% of the variance; 62% from PC1 alone. Figure 4 shows the distribution of princi-pal component scores from each subject along the first 2 PC axes. The shape implied along the PC1 axis depicts a con-tinuum of shapes that ranges from an inverted-U (on the negative side of the abscissa) to a V-shape (on the positive side of the abscissa). The PC2 along the ordinate describes a shape change that goes from NCO contraction (up-in) on the negative side to NCO expansion (down-out) on the positive side (Fig. 4). The intersection of PC1 and PC2 represents the consensus shape of the ppRPE-layer semi-landmarks for all specimens. The PC plot shows 2 distinct clusters (pONSM and normals) that segregate along PC 1. With one notable exception (patient 11), nearly all subjects with pONSM exhibit some degree of the inverted-U shape deformation to relative flattening compared with the nor-mals. There was no obvious segregation of the 2 groups along PC2. The probability that this difference in shape between pONSM and normal subjects could have arisen by chance was 1 in 10,000 permuted data or P = 0.0001. Sibony et al: J Neuro-Ophthalmol 2014; 34: 130-136 133 Original Contribution Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. There was no statistically significant correlation between shape variables and the age of the subject (r = 0.67), disc height (r = 0.67), mean RNFL (0.51), length of the tumor (r = 0.61), proximity of the tumor to the globe (0.66), or length + proximity (r = 0.71). An algorithm that assigned points based on proximity to the globe plus tumor length (in millimeters) did show a moderate correlation (r = 0.75, P = 0.037) with shape. DISCUSSION This study shows that shape of the ppRPE-layer in patients with pONSM differs from normals, and this difference was statistically significant. It is characterized by an inward deformation of the ppRPE-layer toward the vitreous that presumably reflects the shape of the underlying load bearing peripapillary sclera (15) and correlates with both the size and proximity of the tumor to the globe. Larger tumors contiguous to the sclera are associated with greater amounts of deformation. The shape of the ppRPE-layer in 1 patient with a small tumor, most distant from the globe, showed no deformation and was otherwise normal. The peripapillary shape deformation demonstrated on the SD-OCT can, at times, be seen on an MRI, CT, or B-scan echography as flattening of the globe in some cases associated with acquired hyperopia and choroidal folds (22-28). The SD-OCT however is more sensitive and pro-vides greater detail than the MRI and CT. The application of GM to these images can statistically distinguish shape differences from normals even when differences appear nor-mal by gross inspection (15). Pathologically, ONSM may infiltrate the optic nerve head and the adjacent choroid (29-31). Shape deformation in such instances probably is due to direct compression of the optic nerve with axonal flow blockade and proximal swelling, in much the same way that an intraconal orbital FIG. 3. A. Scatter plot shows semi-landmarks from 10 patients, 11 eyes with presumed optic nerve sheath meningioma (pONSM) (black dots) and 30 normal subjects (red dots) after Procrustes superimposition (i.e., after normalizing for location, size, and rotational differences between subjects). B. Thin-plate spline compares the consensus (mean) shape of the peripapillary retinal pigment epithelium-Bruch's membrane (ppRPE) layer in normals with those with pONSM. Nasal is positioned on the right side and temporal is on the left side of the figure. The ppRPE-layer in pONSM has an asymmetric inverted-U shape that is inwardly bowed toward the vitreous and skewed nasally. Normals have a relatively symmetrical outward V-shaped RPE layer directed away from the vitreous. FIG. 4. Principal component analysis shows that 81% of the shape variance among all subjects can be explained by the first 2 principal components (PC1, 62%; PC2, 19%). The shape implied along PC1 (abscissa) displays an inverted U-shape on the negative side to a V-shape on the positive side. PC2 (ordinate) implies a radial expansion or contrac-tion of the neural canal opening. Black-filled circles repre-sent the PC scores of the meningioma patients and open circles represent normals. With one exception (11), the meningioma patients form a distinct cluster (oval) along the negative side of PC1. Normals are more tightly clustered along the positive side of PC1. There was no clear segre-gation between groups along PC2. One patient (11) had a small meningioma approximately 15 mm from the globe with no signs of shape deformation. 134 Sibony et al: J Neuro-Ophthalmol 2014; 34: 130-136 Original Contribution Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. tumor will compress the globe and induce choroidal folds and hyperopia. However, the mass effect on the globe with most pONSM, even those contiguous to the globe, is mild by comparison. Moreover, in 5 of 11 eyes (patients 4, 7, 8, 9, and 10) the deformation was evident even when the tumor did not appear (based on MRI) to directly compress the globe. Taban et al (28) have described a patient with remote parasellar meningioma involving the optic canal and orbital apex, who exhibited choroidal folds and flattening of the globe by B-scan ultrasound. The mechanism by which an ONSM can deform the globe is unknown. It is noteworthy that the shape deforma-tion in pONSM is indistinguishable from the shape of the ppRPE-layer in patients with intracranial hypertension and papilledema. Eight eyes of our patient cohort had optic disc edema at presentation. However, disc edema alone does not explain these shape deformations because we have previously shown that there is no shape deformation in patients with disc edema due to anterior ischemic optic neuropathy (15). In an animal model, Morgan et al (7) have shown that dis-placements of the optic disc surface is probably the result of translaminar pressure differences between the subarachnoid and intraocular fluid compartments. This is the likely expla-nation of the subsurface deformations at the level of the ppRPE-layer in patients with papilledema (15,32). There are a number of similarities in the clinical signs of both chronic papilledema and pONSM. Patients with papilledema initially present with bilateral or asymmetric disc edema, normal acuity and color vision, and enlargement of the blind spot on visual fields. Likewise, patients with meningi-omas of the optic nerve sheath present early on with isolated unilateral optic disc edema, normal acuity, and enlargement of the blind spot, and then slowly progress with loss of peripheral visual field, and eventual optic atrophy and shunt vessels on the disc surface (33-36). In the absence of a large intracranial tumor component, patients with isolated intraorbital pONSM do not have intracranial hypertension. The clinical similarities in their effects on the nerve head between chronic papilledema and pONSM may be a consequence of the underlying bio-mechanics common to both of these entities. Some investigators (37-43) have suggested that the cere-brospinal fluid (CSF) in the perioptic subarachnoid space (poSAS) may not freely communicate with the intracranial subarachnoid space based on measurable concentration gra-dients of CSF proteins and contrast along the optic nerve sheath. This concentration gradient has similarly been dem-onstrated in a patient with an ONSM (38). It is possible that the shape differences in pONSM are the result of localized increased pressure within the poSAS because the tumor effectively functions as a one-way hydraulic valve. The biomechanical effects of the meningioma on the optic nerve sheath may also play a role. Strain is a measure of local deformation of a material or tissue induced by stress (applied force per cross-sectional area). The amount of strain is also influenced by the material properties of the tissue; that is, its ability to resist deformation (stiffness or compliance). Normally, the intraorbital segment of the optic nerve is slack and compliant; the ends fixed within the neural canal and the annulus. Eye movements stress and strain the nerve and the peripapillary eye wall. Thickening, calcification, and increased pressure in the poSAS in patients with meningiomas presumably stiffen the optic nerve sheath. This decrease in compliance may also contribute, if not cause, the deformation observed on OCT. The functional significance of this deformation is unknown. 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