Can Corneal Biomechanical Properties Give Clues About Elasticity of Optic Nerve Scleral Component in Nonarteritic Anterior Ischemic Optic Neuropathy?

The initial symptoms of myasthenia gravis are usually ptosis and diplopia. The diagnosis is often confirmed by testing for anti-acetylcholine receptor antibodies or by observing the effects of intravenous edrophonium (Tensilon) injection. However, these standard tests may be negative in patients with isolated ocular findings. We present the case of an 83-year-old woman with negative serologic and Tensilon testing. She was asked to photograph herself daily. The resulting sequence of daily selfies captured striking fluctuations in her ocular alignment and ptosis. Daily selfies may be a useful strategy for confirming the clinical diagnosis of ocular myasthenia gravis.

Original Contribution Can Corneal Biomechanical Properties Give Clues About Elasticity of Optic Nerve Scleral Component in Nonarteritic Anterior Ischemic Optic Neuropathy? Betul S. Uysal, MD, Fatma Yulek, MD, Pinar Nalcacioglu, MD, Ozge Sarac, MD, Mucella A. Yorgun, MD, Nurullah Cagil, MD Objective: To investigate corneal biomechanical properties among individuals with unilateral nonarteritic anterior ischemic optic neuropathy (NAION) compared to healthy genderand age-matched subjects. Methods: The study subjects were separated into 2 groups: 66 eyes of 33 patients with unilateral NAION (study group) and 33 eyes of 33 healthy individuals (control group). Reichert ocular response analyzer (Reichert Ophthalmic Instruments) was used to assess corneal hysteresis (CH), corneal resistance factor (CRF), cornealcompensated intraocular pressure (IOPcc), and Goldmanncorrelated intraocular pressure values. Also, central corneal thickness was measured using Scheimpflug camera combined with a Placido disc corneal topographer (Sirius; Costruzioni Strumenti Oftalmici). Results: Mean CH and median CRF values were significantly lower in the affected eyes (8.8 ± 1.8 mm Hg, 9.4 mm Hg, respectively) and contralateral unaffected eyes (9.1 ± 1.6 mm Hg, 9.8 mm Hg, respectively) of NAION patients than those in the control group (9.9 ± 1.3 mm Hg, 10.4 mm Hg, respectively; all P , 0.017). Mean IOPcc was significantly higher in the affected eyes of NAION patients (19.2 ± 3.5 mm Hg) than in the eyes of control group (17.1 ± 3.6 mm Hg; P = 0.002). Conclusions: CH and CRF are significantly reduced in patients with NAION, possibly indirectly reflecting structural weakness in the lamina cribrosa. Journal of Neuro-Ophthalmology 2016;36:285-289 doi: 10.1097/WNO.0000000000000406 © 2016 by North American Neuro-Ophthalmology Society Department of Ophthalmology (BSU, OS, MAY), Ankara Ataturk Training and Research Hospital, Ankara, Turkey; and Department of Ophthalmology (FY, PN, NC), Ankara Ataturk Training and Research Hospital, Yildirim Beyazit University, Ankara, Turkey. The authors have no funding or conflicts of interest to disclose. Address correspondence to Betul S. Uysal, MD, Department of Ophthalmology, Ankara Ataturk Training and Research Hospital, Bilkent, Ankara 06800, Turkey; E-mail: [e-mail] Uysal et al: J Neuro-Ophthalmol 2016; 36: 285-289 N onarteritic anterior ischemic optic neuropathy (NAION) is the most prevalent form of optic neuropathy in individuals older than 50 years with an estimated incidence of 2.3-10.2 cases per 100,000 per year (1). Despite well-characterized clinical signs and manifestations, pathophysiology of NAION remains unclear. Risk factors include hypertension and other systemic vascular diseases, diabetes mellitus, and hyperlipidemia (2,3). In addition, the majority of individuals who develop NAION have a structurally complex, crowded optic disc commonly described as a disc at risk (4). The connection between this particular anatomical variation and ischemia remains unclear. An ocular response analyzer (ORA) (Reichert Ophthalmic Instruments, Depew, NY) measures the corneal response to indentation using a noncontact rapid air pulse in vivo. The intraocular pressure (IOP) is measured by the air pressure required to applanate the central cornea. The 2 measurements of the corneal response to the pulse of air are recorded. The force-in applanation (P1) is the force required to flatten the cornea while the air pressure rises, and force-out applanation (P2) is the force at which the cornea becomes flat again while the air pressure declines. P2 has been measured lower than P1 and the difference between the 2 pressures is referred to corneal hysteresis (CH). CH represents the corneal tissue's response to dynamic deformation and is used to determine the "viscous damping" of the cornea (5,6). Corneal resistance factor (CRF) is derived from the formula (P1-k$P2), and it is an artificial parameter reflecting the elasticity and resistance of the cornea (5,6). The ORA also measures corneal-compensated IOP (IOPcc), which is independent of corneal thickness and is not influenced by other properties of the cornea (7). The external covering of the eye is composed of the cornea and sclera, a robust and thick extracellular matrix of collagen and other glycoproteins. Changes in the structure and function of sclera and cornea are interrelated with 285 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution changes in other parts of the eye. Alteration in the mechanical properties of one structure is linked to changes in the properties of the integrated tissue coat (8-10). Kotecha et al (11) suggested that the structural properties of the optic nerve head (ONH) are reflected in the biomechanical properties of the cornea. Thus, an understanding of the probable differences in the corneal biomechanics between individuals with and without NAION may give a clue about susceptibility of ONH and thus help to better understand the pathogenesis and risk factors of NAION. We designed a clinical study to evaluate the corneal biomechanical properties among individuals with unilateral NAION compared to healthy, gender- and age-matched research subjects. MATERIALS AND METHODS Design and Study Population This prospective, cross-sectional, designed, case-control study was conducted at the Yildirim Beyazit University Ankara Ataturk Training and Research Hospital, Department of Ophthalmology. It was reviewed and approved by the local ethics committee according to the standards set forth in the Declaration of Helsinki. All study participants were informed regarding the aims of the study, and written consent was provided by all study participants. Patients with unilateral NAION and healthy subjects were enrolled in this study. These individuals were separated into 2 groups: a study group consisting of both eyes (33 affected and 33 unaffected eyes) of 33 patients with unilateral NAION, and a control group consisting of 33 eyes of 33 healthy individuals. All subjects included in the study group were diagnosed with NAION and were examined at a follow-up appointment. NAION diagnosis was defined as acute and painless visual acuity loss, visual field defects, an ipsilateral relative afferent pupillary defect, color vision deficit, and optic disc edema with hemorrhages. Patients with arteritic anterior ischemic optic neuropathy were excluded based on the clinical findings and laboratory results, including a normal C-reactive protein level and erythrocyte sedimentation rate. The control group was composed of 33 age- and gendermatched subjects who were examined consecutively in the ophthalmology department for a routine examination. The inclusion criteria were intraocular pressure of less than 21 mm Hg for both eyes, normal Humphrey SITA 24-2 visual fields, normal-appearing optic discs, open anterior chamber angles, and no history of any systemic disease. Individuals with a family history of glaucoma, best-corrected visual acuities less than 20/30, or any ophthalmic abnormalities other than refractive errors also were excluded. The following exclusion criteria for all subjects were applied: subjects with unreliable optic disc images, refractive error or astigmatism of greater than 3 diopters, a history of 286 contact lens use, connective tissue disorders, history of corneal or intraocular surgery, ocular injuries, glaucoma, corneal scarring, and corneal pathologies potentially affecting the measurement of biomechanical parameters of the cornea or corneal thickness. Examination Protocol and Measurements Clinical data including demographic features (age, gender, and disease duration) were collected from all participants. All participants underwent full neuro-ophthalmologic examination, including best-corrected visual acuity, pupil diameter, pupillary light reaction, evaluation for the presence of relative afferent pupillary defect, color vision testing with Ishihara plates, slit-lamp examination of the anterior ocular segment, IOP measurement with Goldmann applanation tonometer (IOP-GAT), and funduscopy. CH, CRF, IOPcc, and Goldmann-correlated IOP (IOPg) were assessed using the ORA. The fundamentals of this device have been described in greater detail elsewhere (5). Other studies have demonstrated a high degree of reproducibility using this technique (6). Patients were asked to stare at a blinking red light while at least 2 measurements were performed on each eye. High-quality wavelength scores of 7 or greater were used in the analysis. Raw data were examined and controlled for the presence of welldefined applanation peaks located above the pressure curve. A Scheimpflug camera with a Placido disc corneal topographer (Sirius; Costruzioni Strumenti Oftalmici, Florence, Italy) was used to measure central corneal thickness (CCT). The optimal alignment was determined from 3 replicate measurements. An experienced clinician performed all measurements according to the current standards of normal clinical practice and the manufacturer's (Reichert) guidelines for the ORA. All examinations were made between 9:00 AM and 11:00 AM. The clinician was masked to the study group assignments. Statistical Analysis Both the affected and unaffected eyes were included for all patients in the NAION group; only the right eye data were included for individuals in the control group. All data analysis was performed using SPSS v11.5 for Windows (SPSS, Inc, Chicago, IL). The distribution of continuous variables was assessed relative to a normal distribution using the Kolmogorov-Smirnov test. Continuous variables are reported as mean ± standard deviation or median (range). Differences between the study group and the control group were evaluated using the Student t test for normally distributed variables and the Mann-Whitney U test for nonnormally distributed variables. Differences in the clinical parameters between healthy and NAION-affected eyes were evaluated in the patient group using the paired samples t test for normally distributed variables and using the Wilcoxon signed-rank test for nonnormally distributed variables. The Pearson x2 test was used to analyze differences in Uysal et al: J Neuro-Ophthalmol 2016; 36: 285-289 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution nominal data. The threshold of statistical significance was set P , 0.05. But, for all possible multiple comparisons, the Bonferroni correction was applied for controlling Type I error, and P , 0.017 was accepted as statistically significant. Sample Size Estimation A total sample size of 58 (29 per group) was required to detect at least 0.9 difference in CH between the groups with a power of 80% at the 1.67% significance level owing to the Bonferroni correction. The 0.9 difference was taken from both our pilot study and clinical experiments. Sample size estimation was performed using NCSS and PASS 2000 software (NCSS, Kaysville, UT). RESULTS Demographic Characteristics of the Subjects Demographic characteristics of the patients with NAION and healthy control subjects are summarized in Table 1. Gender distribution and age did not differ between the 2 groups (P = 0.278 and P = 0.138, respectively). The mean time elapsed since diagnosis was 12.8 ± 5.0 months (range, 7-22 months) in the study group. Comparison of ORA Parameters, IOP-GAT, and CCT Values Clinical measurements of the study and control groups including CH, CH, IOPcc, IOPg, IOP-GAT, and CCT are summarized in Table 2. Mean CH was 8.8 ± 1.8 mm Hg in the affected eyes of NAION patients and 9.9 ± 1.3 mm Hg in the control group, and this difference was significant (P = 0.001). Median CRF value was significantly lower in the affected eyes of NAION patients (9.4 mm Hg) relative to the control group (10.4 mm Hg; P = 0.002). Mean IOPcc values in the affected eyes in the study group and control group were 19.2 ± 3.5 and 17.1 ± 3.6 mm Hg, respectively, a significant difference (P = 0.002). IOPg, IOP-GAT, and CCT did not differ significantly between the affected eyes of NAION patients and the control group (P . 0.017). Average CH was 9.1 ± 1.6 mm Hg in the unaffected eyes of NAION patients and 9.9 ± 1.3 mm Hg in the healthy TABLE 1. Demographic characteristics of patients with NAION (study group) and control group Variable Study Group Control Group (n = 33) (n = 33) P value Age, y, mean ± SD 61.3 ± 10.4 64.1 ± 10.1 Gender, n (%) Male 21 (63.6) 15 (45.5) Female 12 (36.4) 18 (54.5) *Student t test. † Pearson x2 test. NAION, nonarteritic anterior ischemic optic neuropathy. Uysal et al: J Neuro-Ophthalmol 2016; 36: 285-289 0.278* 0.138† subjects (P = 0.002). Median CRF was significantly lower in the unaffected eyes of NAION patients (9.8 mm Hg) than in the control subjects (10.4 mm Hg, P = 0.003). IOPcc, IOPg, IOP-GAT, and CCT did not differ significantly between the healthy subjects and the unaffected eyes of the NAION patients (P . 0.017). Among the NAION patients, CH, CRF, IOPcc, IOPg, IOP-GAT, and CCT did not differ significantly between the affected eye and the contralateral unaffected eye (P . 0.017). DISCUSSION Compartment syndrome has been proposed as a causative factor in patients with NAION initiated by ONH capillary dysregulation, especially in individuals with a disc at risk (12). In compartment syndrome, concentrated edema results in mechanical pressure on optic nerve (ON) fibers, blockage of axonal transport, and compression of the local circulation (13). Few histopathological studies of the ON have been conducted in patients with NAION. Tesser et al (14) described an infarction in a patient with clinically confirmed NAION (20 days post onset) that was not linked to specific vasculature but instead appeared to be due to a compartment syndrome. In another study (15), 69 of 193 eyes (36%) with ON ischemia exhibited laminar region cavernous degeneration, consistent with compartment syndrome as a mechanism of ischemia. We hypothesized that CRF and CH might be altered in NAION patients, possibly indirectly reflecting the weakness of the lamina cribrosa, which might play a role in the compartment syndrome. To our knowledge, biomechanical properties of the cornea have not been reported previously in patients with NAION. The present study demonstrated that the affected and unaffected eyes of unilateral NAION patients exhibit significantly lower CH and CRF compared to the eyes of healthy control subjects. Kamiya et al (16) and others (17,18) reported that CH is independent of gender, age, manifest refraction, and keratometric changes; however, some studies showed that CH and CRF slightly decrease with increasing age in healthy adults (6,19). The CH and CRF value of our control subjects aged 64.1 ± 10.1 years were 9.9 ± 1.3 and 10.4 mm Hg (range, 7.7-13.5 mm Hg), respectively, in this study. The reason for discrepancies in CH and CRF values with increasing age is unclear. Given that the cornea, sclera, peripapillary ring, and lamina cribrosa in an individual eye are essentially made from extracellular matrix constituents, their biomechanical characteristics might be similar. This biomechanical similarity has reported in some experimental studies (8,9). Also, most studies with several types of glaucoma have suggested that CH and CRF may be an indirect measure of the viscoelastic properties of the posterior segment of the eye, especially the lamina cribrosa and peripapillary sclera, which are the primary supporting structures of the ONH 287 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 2. Comparison of the ocular response analyser measurements, IOP measurement with Goldmann applanation tonometer, and CCT in the affected and unaffected eyes of patients with NAION (study group) and controls Variable CH (mm Hg), mean ± SD CRF (mm Hg), median (min-max) IOPcc (mm Hg), mean ± SD IOPg (mm Hg), mean ± SD IOP-GAT (mm Hg), mean ± SD CCT (mm), median (min-max) Unaffected Eyes of Study Control Group Affected Eyes of (n = 33) P value†‡ P value†§ Study Group (n = 33) Group (n = 33) P value*† 8.8 ± 1.8 9.4 (5.0-12.2) 19.2 ± 3.5 16.9 ± 5.3 17.0 ± 2.1 540 (491-573) 9.1 ± 1.6 9.8 (6.0-13.0) 18.0 ± 4.4 16.0 ± 4.3 16.1 ± 3.5 542 (474-594) 0.144k 9.9 ± 1.3 0.153k 10.4 (7.7-13.5) 0.243k 17.1 ± 3.6 0.163k 17.0 ± 3.3 0.155k 17.0 ± 2.2 0.833** 548 (491-593) 0.002¶ 0.003# 0.042¶ 0.081¶ 0.075¶ 0.249# 0.001¶ 0.002# 0.002¶ 0.309¶ 0.519¶ 0.239# Bold indicates significant P values (P , 0.017). *Comparisons between the affected eyes and the contralateral unaffected eyes within the study group. † The results of P value that are ,0.017, according to the Bonferroni correction, was considered statistically significant. ‡ Comparisons between the unaffected eyes within the study group and the control group. § Comparisons between the affected eyes within the study group and the control group. k Paired t test. ¶ Student t test. # Mann-Whitney U test. ** Wilcoxon signed-rank test. CCT, central corneal thickness; CH, corneal hysteresis; CRF, corneal resistance factor; IOP, intraocular pressure; IOPcc, cornealcompensated intraocular pressure; IOPg, Goldmann-correlated intraocular pressure; IOP-GAT, intraocular pressure measurement with Goldmann applanation tonometer; NAION, nonarteritic anterior ischemic optic neuropathy. (11,20-26). Compression and deformation of the lamina cribrosa and subsequent retinal ganglion cell damage have been reported in the glaucomatous optic neuropathy (27). Recent studies have shown decreased damping capacity of the cornea (indirectly reflecting low damping capacity of the lamina cribrosa) in glaucomatous eyes (20-24) and demonstrated an association between low CH and glaucomatous progression (25,26). Laminar thickness was found thinner in normal tension glaucoma patients in comparison to primary open-angle glaucoma patients (28). In addition, CH and CRF were significantly lower in eyes with progressive normal tension glaucoma, presumably reflecting the structural weakness in the lamina cribrosa (29). In light of these studies, we believe that the biomechanical parameters of the cornea (CH and CRF) indirectly reflecting the structural features of the lamina cribrosa, which might play a role in the compartment syndrome. Eyes with lower CH have low capability of damping the IOP changes compared to those with higher CH (30). The lamina cribrosa cannot properly absorb increased mechanical pressure in eyes with lower hysteresis. The resulting deformation and stress on the ON fibers and vasculature may cause damage in NAION patients. Consequently, low damping capacity of the lamina cribrosa, which is indirectly measured by low CH, might increase the effect of compartment syndrome in the eyes of NAION patients. Patients with NAION in a single eye have a 15%-19% chance of developing NAION in the contralateral eye within 5 years (31). We also found significantly lower CH and CRF values in the contralateral unaffected eyes of patients with unilateral NAION compared to healthy subjects. Therefore, 288 our findings might reflect an underlying risk factor for the development of NAION. In our study, CCT was lower in both affected and contralateral unaffected eyes of patients with unilateral NAION patients relative to the healthy control subjects, although this observation did not reach the level of statistical significance. Similar results were found in a previous study (32). A direct correlation has been found between CCT and biomechanical parameters of the cornea, including CH and CRF (16,33). The findings of our study revealed that CH and CRF were lower in NAION patients compared to control group, whereas there was no difference in CCT values between all groups. Consequently, our results suggest that differences in CH and CRF might be attributable to biomechanical and structural differences in the cornea between these groups, rather than differences in corneal thickness measurements. There are some limitations in our study. First, the measurements were done at several time points following the occurrence of NAION. It is possible that the values of the parameters we measured (CH and CRF) were altered by the ischemic event. Second, we do not know the clinical significance of the difference in CH and CRF values, although our results are statistically significant. Third, the control subjects also may be potentially at risk for developing NAION, although we carefully selected individuals without any known optic nerve pathology. In conclusion, the present study demonstrated that CH and CRF are significantly reduced in patients with NAION, presumably associated with structural weakness in the lamina cribrosa. Structural vulnerability in the ONH may Uysal et al: J Neuro-Ophthalmol 2016; 36: 285-289 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution facilitate the compartment syndrome effect, exacerbating the ischemic damage. Prospective cohort studies are needed to elucidate the relationship between corneal biomechanics and NAION pathogenesis. Demonstration of this potential connection would be an important step in identifying risk factors for developing NAION. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: B. S. Uysal, F. Yulek, N. Cagil; b. Acquisition of data: B. S. Uysal; c. Analysis and interpretation of data: F. Yulek, M. A. Yorgun. Category 2: a. Drafting the manuscript: B. S. Uysal, F. Yulek; b. Revising it for intellectual content: F. Yulek, P. Nalcacioglu, O. Sarac. Category 3: a. Final approval of the completed manuscript: F. Yulek, P. Nalcacioglu. REFERENCES 1. 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