Optic Nerve Angle in Idiopathic Intracranial Hypertension

The tortuosity of the optic nerve can be quantified radiologically by measuring the angle of optic nerve deformation (the "optic nerve angle" [ONA]). In patients with idiopathic intracranial hypertension (IIH), lowering the intracranial pressure (ICP) to a normal range by lumbar puncture leads to straightening of the optic nerve and an increase in the measured sagittal ONA on MRI. It is uncertain whether there is any correlation between ONA and cerebrospinal fluid (CSF) opening pressure or visual function

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Optic Nerve Angle in Idiopathic Intracranial Hypertension Benson S. Chen, MBChB, FRACP, Solmaz Asnafi, MD, Mung Y. Lin, BS, Beau B. Bruce, MD, PhD, Jane H. Lock, MBBS, FRANZCO, Rahul A. Sharma, MD, MPH, Nancy J. Newman, MD, Valérie Biousse, MD, Amit M. Saindane, MD, MBA Background: The tortuosity of the optic nerve can be quantified radiologically by measuring the angle of optic nerve deformation (the “optic nerve angle” [ONA]). In patients with idiopathic intracranial hypertension (IIH), lowering the intracranial pressure (ICP) to a normal range by lumbar puncture leads to straightening of the optic nerve and an increase in the measured sagittal ONA on MRI. It is uncertain whether there is any correlation between ONA and cerebrospinal fluid (CSF) opening pressure or visual function. Methods: Retrospective study of patients with and without IIH who had MRI of the brain followed by lumbar puncture with CSF opening pressure within 24 hours of MRI. Before LP and within 24 hours of MRI of the brain, all patients with IIH had neuro-ophthalmologic assessment including visual acuity, Humphrey Visual Field (HVF), and fundus photography. Sagittal ONA was measured on multiplanar T2-SPACE images on a DICOM viewer. Papilledema on the fundus photographs was graded using the Frisén scale. Results: Fifty-four patients with IIH and 30 unmatched controls were included. The IIH group was 6.3 years younger (95% CI 2.4–10.3, P = 0.002), had 8.7 kg/m2 higher body mass index (4.9–12.5, P , 0.001), and 26.3% more women (P = 0.011) compared with controls. In both eyes, the ONA was significantly smaller in patients with IIH by 12° compared with controls (7°–17°, P , 0.00001). In the IIH Departments of Ophthalmology (BSC, MYL, BBB, JHL, RAS, NJN, VB), Radiology and Imaging Sciences (SA, AMS), Epidemiology (BBB), Neurology (BBB, NJN, VB), and Neurological Surgery (NJN), Emory University, Atlanta, Georgia. B. S. Chen is the recipient of the V. J Chapman Research Fellowship, awarded by the Neurological Foundation of New Zealand. B. B. Bruce is a medicolegal consultant for Bayer and individual litigants on the topic of idiopathic intracranial hypertension. V. Biousse and N. J. Newman are consultants for GenSight Biologics. They are supported in part by an unrestricted departmental grant (Department of Ophthalmology) from Research to Prevent Blindness, Inc, New York, by NIH/NEI core grant P30-EY06360 (Department of Ophthalmology, Emory University School of Medicine), and by NIH/ NINDS (RO1NSO89694). N. J. Newman is a consultant for Santhera Pharmaceuticals and Stealth BioTherapeutics. The remaining authors report no conflicts of interest. Address correspondence to Amit M. Saindane, MD, Department of Radiology and Imaging Sciences, Emory University School of Medicine, 1364 Clifton Road NE, Suite BG20, Atlanta, GA 30322; E-mail: [e-mail] e464 group, no correlation between ONA and the CSF opening pressure was present in either eye (right eye r = 0.19, P = 0.15; left eye r = 0.18, P = 0.19) The ONA did not correlate with logarithm of the minimum angle of resolution visual acuity (right eye r = 0.26, P = 0.063; left eye r = 0.15, P = 0.27), HVF mean deviation (right eye r = 0.0059, P = 0.97; left eye r = 20.069, P = 0.63), or Frisén grade (Spearman’s rho right eye 0.058, P = 0.67; left eye 0.14, P = 0.30). Conclusions: The ONA is significantly smaller in patients with IIH compared to controls, but does not correlate with CSF opening pressure, severity of papilledema, or visual function. The ONA may be useful in identifying patients with raised ICP, but not necessarily those with a poor visual prognosis. Journal of Neuro-Ophthalmology 2021;41:e464–e469 doi: 10.1097/WNO.0000000000000986 © 2020 by North American Neuro-Ophthalmology Society O ptic nerve tortuosity and distension of the optic nerve sheath on MRI have been described in the setting of idiopathic intracranial hypertension (IIH) (1–4). The degree of optic nerve tortuosity has been studied previously by measuring the greatest bend of the optic nerve (“optic nerve angle” [ONA]) in the sagittal and axial planes on multiplanar T2 SPACE images on MRI (5,6). One study found a significant difference in the ONA measurements of patients with IIH compared with a control group without intracranial hypertension (5). An additional prospective study of patients with IIH undergoing lumbar puncture with MRIs obtained before and after lumbar puncture found that the ONA on pre– and post–lumbar puncture MRI was associated with the cerebrospinal fluid (CSF) pressure status of the patient (6). All patients initially had elevated CSF pressure. Reduction of CSF pressure into the normal range by lumbar puncture immediately resulted in a significant reduction in the sagittal and axial bend of the optic nerve, with a corresponding increase in the measured ONA. It is uncertain whether ONA correlates directly with CSF pressure or whether a relationship exists between ONA Chen et al: J Neuro-Ophthalmol 2021; 41: e464-e469 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution and clinical findings such as papilledema or visual function. Other studies have found an association between papilledema and CSF pressure (7) and visual function (8), with a high grade of papilledema being associated with an elevated CSF pressure $350 mm H2O (7), and worse presenting and final visual outcomes (8). If a clear relationship between ONA and CSF pressure exists, ONA measurements could be used to noninvasively assess intracranial pressure (ICP) status, avoiding invasive procedures such as lumbar puncture. In addition, if a correlation between the ONA and papilledema severity exists, ONA measurements may enable clinicians to identify patients who are most at risk of vision loss to institute more aggressive treatment or closer follow-up. We sought to explore the relationship between ONA, CSF pressure, severity of papilledema, and visual function in patients with and without IIH. METHODS Patients This retrospective study was approved by our institutional review board. Patients with IIH were identified retrospectively from an electronic medical record search of patients 18 years and older presenting to our institution between August 2016 and September 2019, with a diagnosis of IIH made by one of 3 expert neuro-ophthalmologists. Patients with IIH were included if they met the most recent diagnostic criteria (1), had an assessment by a neuroophthalmologist with definite papilledema, and had contrast-enhanced MRI brain at our institution performed within 24 hours before lumbar puncture with a CSF opening pressure $25 cm H2O. Patients in the control group were identified retrospectively from an electronic medical record search for patients aged 18 years and older who had undergone MRI brain and fluoroscopic-guided lumbar puncture on the same visit at our institution. To exclude subjects with ICP disorders or preexisting pathology involving the optic nerves, a review of the MRI report and electronic medical records was performed and patients were excluded if there was a history of headache or intracranial abnormalities that would predispose to raised ICP, any history suggestive of an optic neuropathy such as previous optic neuritis, if the clinical indication for the MRI was suggestive of raised ICP, if there were imaging features of raised ICP or optic nerve abnormalities on MRI, or if the CSF opening pressure was $25 cm H2O. The age, sex, and body mass index of all patients was obtained by review of medical records. Neuro-Ophthalmology Assessment and Fundus Photography All patients with IIH were examined by an expert neuroophthalmologist before the MRI and lumbar puncture. Chen et al: J Neuro-Ophthalmol 2021; 41: e464-e469 Examination included assessment of Snellen visual acuity (converted to logarithm of the minimum angle of resolution [logMAR] acuity) and 24-2 SITA-Fast Humphrey visual field (HVF) (mean deviation recorded in decibels). A fundus photograph of each eye was taken by a professional photographer using the TRC-50DX mydriatic retinal camera (Topcon, Tokyo, Japan) after pharmacologic dilatation of the pupils, as routinely performed at our institution. The fundus photographs were deidentified and the severity of papilledema in each eye graded by 2 neuro-ophthalmologists, masked to the MRI findings and the CSF pressure, according to the modified Frisén scale (9). If the 2 neuro-ophthalmologists were unable to agree on the grade of papilledema, the final grade was determined by a third neuro-ophthalmologist. Imaging and Lumbar Puncture Protocol All patients underwent MRI on a 3-T (Tim Trio; Siemens, Erlangen, Germany) or 1.5-T unit (Avanto or Espree; Siemens) in the supine position. The MRI protocol included sagittal T2 Sampling Perfection with Application optimized Contrasts using different flip angle Evolution (SPACE) using used the following parameters for all patients: time to recovery 1,500 ms, time to echo 226 ms, flip angle 100, field of view 22.5 cm, matrix 256 · 256, and slice thickness 1.5 mm. Patients in the IIH group had a fluoroscopically guided lumbar puncture by a neuroradiologist using a standardized technique reported previously (6). Opening pressure was measured using CSF manometry and recorded to the nearest centimeter of water. Imaging Analysis ONA was measured by 2 of the study investigators independently, masked to the demographics, CSF pressure, and grade of papilledema of each patient set, using the technique previously reported (6). ONA measurement was performed on anonymized and randomized multiplanar T2 SPACE images using a DICOM viewer (Osirix; Pixmeo, Bernex, Switzerland). Oblique sagittal images were rendered using a multiplanar reformat tool to depict the optic nerve in its longest continuous profile. The angle of the greatest bend in the optic nerve in the sagittal plane was measured for each eye (Fig. 1A). The angle formed by the long axis of the orbit and the long axis of the globe was also measured to assess for the direction of vertical gaze (Fig. 1B). Statistical Analysis Statistical analysis was performed using R: A language and environment for statistical computing (R Foundation for Statistical Computing, http://www.R-project.org), with significance defined as P , 0.05. Continuous variables were reported as mean and SD or median and IQR. Discrete variables were reported as counts (n) and percentages (%). Mean sagittal ONA measurement was used for further statistical analysis where applicable. e465 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 1. T2 MRI: Sagittal views showing measurement of the greatest bend in the optic nerve (the “optic nerve angle”) (A) and measurement of the vertical gaze angle (B). Correlation between continuous variables was performed with Pearson correlation coefficient. Interobserver agreement for the 2 sagittal ONA measurements was evaluated with intraclass correlation coefficient. Categorical variables were compared between the 2 groups using a Fisher exact test, and continuous variables were compared with a twosample t test. A cutoff for sagittal ONA that simultaneously maximized sensitivity and specificity for raised ICP was calculated by ROC curve analysis using ONA measurements from one eye. RESULTS A total of 54 patients with a diagnosis of IIH and 30 unmatched control patients were enrolled in the study (Table 1). All control patients were identified as having a history of multiple sclerosis without a history of optic neuritis or headache. All had MRI and lumbar puncture as part of the work-up for multiple sclerosis. Compared with the controls, patients with IIH were significantly younger and heavier. There were more women in the IIH group. The median CSF opening pressure in patients with IIH was significantly higher. There was high inter-rater reliability between the 2 study investigators measuring the sagittal ONA, with an intraclass correlation coefficient of 0.82 for the right eye (95% CI, 0.73–0.88) and 0.83 for the left eye (95% CI, 0.76–0.89). In both eyes, the sagittal ONA was significantly smaller in patients with IIH compared with controls by 12o (95% CI, 7°–17°, P , 0.001) (Fig. 2). After controlling for age, sex, and BMI, the sagittal ONA remained significantly smaller among patients with IIH (right eye P , 0.001; left eye P = 0.001) and none of the other variables were a significant predictor of the ONA. There was no difference in the mean vertical gaze angle difference in either eye between patients with IIH and controls (right eye 95% CI, 20.89° to 9.41°, P . 0.10; left eye 95% CI, 20.84° to 9.88°, P . 0.05). A sagittal ONA cutoff of 164.5° provided the best balance between predicted sensitivity (66.7%) and specificity (66.7%) (AUC 0.79; 95% CI, 0.69–0.90), with a positive likelihood ratio of 2. Patients with IIH had a median logMAR visual acuity of 0 (Snellen 20/20) in both eyes and median HVF mean deviation of 23.30 dB in the right eye and 23.23 dB in the left eye (Table 2). Most patients with IIH had Frisén grade 3 or higher papilledema, with 65% of patients having grade 3 or higher papilledema in at least one eye. Three patients (5%) had asymmetric papilledema defined as a two-grade or more difference between eyes. In the IIH group, there was no significant correlation between ONA and CSF pressure in either eye (right eye, r = 0.19; left eye, r = 0.18; P . 0.15). ONA did not correlate with logMAR visual acuity (right eye, r = 0.26, P = 0.06; left eye, r = 0.15; P = 0.27), HVF mean deviation (right eye, r = 0.0059; left eye, r=20.069; P . 0.63), or Frisén grade (Spearman’s rho right eye 0.058, P = 0.67; left eye 0.14, P = 0.30). DISCUSSION Increased optic nerve tortuosity on MRI has been reported in patients with IIH. Our study suggests that sagittal ONA, as a quantitative measure of optic nerve tortuosity, can be used to assess ICP status. Patients with IIH in our study had significantly smaller ONA compared with control patients. TABLE 1. Characteristics of IIH and control patients Age, yr Male BMI, kg/m2 CSF-OP, cmH2O IIH Controls P value 33.0 (25.3–38.9) 2 (3.7%) 37.08 (32.83–41.18) 37 (33–42) 39.3 (33.0–44.4) 9 (30%) 28.38 (22.00–31.63) 15 (14–18) 0.002 0.01 ,0.001 0.002 All values displayed as n (%) or median (IQR). BMI, body mass index; CSF-OP, cerebrospinal fluid opening pressure; IIH, idiopathic intracranial hypertension. e466 Chen et al: J Neuro-Ophthalmol 2021; 41: e464-e469 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 2. Dot-and-box plot comparing optic nerve angle (ONA) in the left eye and right eye in patients with idiopathic intracranial hypertension (IIH) and controls (A). T2 MRI: Sagittal views showing a small ONA in a patient with IIH (147°) (B) and a large ONA in a control patient (182°) (C). However, we did not find a strong correlation between CSF opening pressure and ONA. A single sagittal ONA measurement cannot be used to quantify ICP but may indicate a CSF opening pressure of $25 cm H2O if the ONA is 164.5° or less. An ONA that reaches this cutoff increases the patient’s post-test probability of having raised ICP by around 15%. Changes in the tortuosity of the optic nerve appear to be a dynamic process related to ICP status. A previous study demonstrated that patients with intracranial hypotension had significantly decreased CSF in the optic nerve sheath and a larger ONA compared with controls (5). It is likely that intracranial hypotension leads to reduced CSF distension in the perioptic subarachnoid space, resulting in short- ening and straightening of the optic nerve sheath apparatus between the relatively fixed globe and the optic canal. In our study, we speculate that the reverse occurs, with intracranial hypertension causing increased CSF distension, increased bending of the optic nerve sheath apparatus, and a smaller ONA. Although increased optic nerve tortuosity has been reported in patients with IIH, this imaging finding has been reported in about 43% of patients (2). We considered that the optic nerve may be less susceptible to bending when the CSF pressure is only mildly elevated. However, we did not find a correlation between ONA and CSF pressure. Other factors are likely to be important in determining optic nerve tortuosity, such as the size of the optic canal, TABLE 2. Visual function and papilledema grade of patients with IIH logMAR visual acuity HVF, mean deviation; dB Frisén grade 1 2 3 4 5 Right Eye Left Eye 0 (0 to 0.09691) 23.30 (26.91 to 21.12) 0 (0 to 0.09691) 23.23 (26.92 to 21.54) 10 (19%) 8 (15%) 18 (33%) 12 (22%) 6 (11%) 11 (20%) 13 (24%) 8 (15%) 16 (30%) 6 (11%) All values displayed as n (%) or median (IQR). HVF, Humphrey visual field; IIH, idiopathic intracranial hypertension; logMAR, logarithm of the minimum angle of resolution. Chen et al: J Neuro-Ophthalmol 2021; 41: e464-e469 e467 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution duration of ICP elevation, and biomechanical properties of the optic nerve sheath. It is recognized that the size of the optic canal plays an important role in the dynamics of conveying the CSF pressure to the optic nerve sheath (10) and may be important in preventing the development of papilledema and optic nerve tortuosity in the presence of elevated CSF pressure. In addition, the biomechanical properties of the optic nerve sheath, particularly reduced elasticity or increased stiffness, may limit the ability of the nerve to bend. We did not find a relationship between ONA and visual acuity, HVF mean deviation, or Frisén grade. However, most patients with IIH in our study had good visual acuity and HVF mean deviation at the time of their neuroophthalmologic assessment, which may have masked the relationship with the ONA. Nevertheless, papilledema severity and visual function are more likely to be determined by structural changes at the optic nerve head. It has been proposed that elevated ICP induces forces in the retrolaminar subarachnoid space that can deform optic nerve head structures. In patients with IIH, Frisén grade strongly correlates with optical coherence tomography (OCT) parameters including retinal nerve fiber layer thickness, total retinal thickness, and optic nerve head volume (11). Although we have not correlated these OCT parameters with ONA, our study suggests that optic nerve tortuosity is unlikely to play a significant role in altering the biomechanical environment of the peripapillary optic nerve head and, as a consequence, visual function or Frisén grade. A key strength of our study was that all patients with IIH had neuro-ophthalmologic assessment, MRI, and lumbar puncture for CSF opening pressure (precisely in that order) all within a 24-h period. All clinical assessments, neuroimaging acquisition and interpretation, and lumbar punctures were performed in a standardized fashion at one institution, ensuring reliability of data collected. The sagittal T2 SPACE sequence that we used is readily available and part of the standard MRI brain protocol. Although the SPACE sequence is specific to Siemens MRI, an equivalent isotropic 3D sequence is available with other brands of MRI, allowing the ONA to be measured on multiplanar reformats. Another strength is the inclusion of a comparison group without raised ICP. Although patients in the control group did not have raised ICP, they may not be truly representative of a “normal” population. By chance, all patients in the control group were found to have a history of multiple sclerosis or clinically isolated syndrome. However, none had had a history of optic neuritis or optic atrophy. In addition, patients with MRI findings suggestive of raised ICP such as empty sella were excluded even if they had normal CSF opening pressure, as we could not rule out a previous history of raised ICP. A major limitation of this study was inability to control for gaze direction on MRI. A recent study of 10 patients with and without primary open angle glaucoma found that e468 the tortuosity of the optic nerve in the axial plane was significantly affected by direction of gaze (12). The previous study did not determine whether vertical gaze significantly affects the tortuosity of the optic nerve in the vertical plane. Although we were unable to adjust the sagittal ONA measurement for the vertical gaze angle in our study, we did not find a significant difference in vertical gaze angle between patients with IIH and controls in either eye. In a prior study, both the axial and sagittal ONA were found to change significantly after lumbar puncture (6). In our study, we chose to only measure the sagittal ONA for several reasons. Although both measurements had excellent inter-rater agreement in the previous study, sagittal ONA measurements had a higher agreement (0.89) than axial ONA measurements (0.79) (6). We also found that compared with axial ONA measurements, sagittal ONA measurements were straightforward to perform due to greater ease of reformatting an oblique sagittal image to display the optic nerve in a continuous profile. This is the first study to explore the relationship between ONA, CSF pressure, and visual function in patients with and without IIH. The ONA is significantly smaller in patients with IIH compared to controls and may be useful in identifying patients with raised ICP. Our study does not address whether this finding is isolated to patients with IIH or also seen in other conditions with raised ICP. In addition, we do not know whether changes in the ONA occur acutely or slowly in response to chronically raised ICP and whether they persist even after treatment of raised ICP. Further studies measuring the ONA in patients with other conditions causing acutely and chronically raised ICP are required. Finally, the absence of a correlation between sagittal ONA and papilledema may also make measurement of the ONA useful in identifying patients with IIH without papilledema (IIHWOP). In patients without a sixth nerve palsy, a diagnosis of IIHWOP can be suggested in the presence of 3 of 4 MRI features of raised ICP (reduced pituitary gland height, increased optic nerve sheath diameter, flattening of the posterior globe, and transverse venous sinus stenosis) (1). A combination of 3 of 4 MRI features is highly specific (nearly 100%) and moderately sensitive (64%) for raised ICP and suggests IIHWOP in patients with chronic headache and no papilledema (4). Additional studies are required to determine the sensitivity and specificity of sagittal ONA in isolation or in combination with other MRI features of raised ICP, in IIH and IIHWOP. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: B. S. Chen, B. B. Bruce, N. J. Newman, V. Biousse, and A. M. Saindane; b. Acquisition of data: B. S. Chen, S. Asnafi, M. Y. Lin, J. H. Lock, R. A. Sharma, N. J. Newman, V. Biousse, and A. M. Saindane; c. Analysis and interpretation of data: B. S. Chen, S. Asnafi, M. Y. Lin, B. B. Bruce, N. J. Newman, V. Biousse, and A. M. Saindane. Category 2: a. Drafting the manuscript: B. S. Chen, B. B. Bruce, N. J. Newman, V. Biousse, and A. M. Saindane; b. Revising it for intellectual content: B. S. Chen, S. Asnafi, Chen et al: J Neuro-Ophthalmol 2021; 41: e464-e469 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution M. Y. Lin, B. B. Bruce, J. H. Lock, R. A. Sharma, N. J. Newman, V. Biousse, and A. M. Saindane. Category 3: a. Final approval of the completed manuscript: B. S. Chen, S. Asnafi, M. Y. Lin, B. B. Bruce, JL, R. A. Sharma, N. J. Newman, V. Biousse, and A. M. Saindane. 7. 8. REFERENCES 1. Friedman DI, Liu GT, Digre KB. Revised diagnostic criteria for the pseudotumor cerebri syndrome in adults and children. Neurology. 2013;81:1159–1165. 2. Bidot S, Saindane AM, Peragallo JH, Bruce BB, Newman NJ, Biousse V. Brain imaging in idiopathic intracranial hypertension. 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