Title | Optic Disc Drusen in Children: The Copenhagen Child Cohort 2000 Eye Study |
Creator | Lasse Malmqvist, MD; Xiao Qiang Li, MD, PhD; Christina L. Eckmann, MSc; Anne M. Skovgaard, DMSc; Else M. Olsen, MD, PhD; Michael Larsen, MD, DMSc; Inger C. Munch, MD, PhD; Steffen Hamann, MD, PhD |
Affiliation | Department of Ophthalmology (LM, XQL, CLE, ML, SH), Rigshospitalet, University of Copenhagen, Glostrup, Denmark; Faculty of Health and Medical Sciences (LM, ML, ICM, SH), University of Copenhagen, Copenhagen, Denmark; Department of Public Health (AMS, EMO), Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark; National Institute of Public Health (AMS), Faculty of Health Sciences, University of Southern Denmark, Odense, Denmark; and Department of Ophthalmology (ICM), Zealand University Hospital, Roskilde, Denmark. |
Abstract | Optic disc drusen (ODD) are seen in up to 2.4% of the general population, but the etiology and pathophysiology of the condition is still unknown. The purpose of this study was to determine the prevalence of ODD in a population-based child cohort and to determine if scleral canal diameter and fetal birth and pubertal parameters are associated with the presence of ODD. This observational, longitudinal population-based birth cohort study, with a nested case-control, included 1,406 children. Eye examinations were performed when the children were between 11 and 12 years of age. Assessment was performed of optical coherence tomography (OCT) scans from 1,304 children with gradable enhanced depth imaging scans of the optic disc. ODD in one or both eyes were found in 13 (1.0%) of all children. All but one of the cases were found in children with scleral canal diameter in the lowest quartile (1,182-1,399 μm) in the nested case-control study. Children with ODD had a mean disc diameter of 1,339 μm (interquartile range, 30 μm), whereas it was 1,508 μm (interquartile range, 196 μm) in the 130 controls without ODD (P < 0.001). No differences in sex, birth weight, refractive error, and Tanner stages (of puberty) were found between children with and without ODD. The prevalence of ODD was 1% in a large child cohort examined by OCT. ODD was found only in eyes with a narrow scleral canal, which is consistent with the hypothesis that ODD might arise as a consequence of retinal nerve fiber congestion in the scleral canal. |
Subject | Birth Weight; Child; Cohort Studies; Cross-Sectional Studies; Denmark; Female; Follow-Up Studies; Humans; Male; Nerve Fibers; Optic Disk; Optic Disk Drusen; Prevalence; Retinal Ganglion Cells; Sclera; Tomography, Optical Coherence |
OCR Text | Show Original Contribution Optic Disc Drusen in Children: The Copenhagen Child Cohort 2000 Eye Study Lasse Malmqvist, MD, Xiao Qiang Li, MD, PhD, Christina L. Eckmann, MSc, Anne M. Skovgaard, DMSc, Else M. Olsen, MD, PhD, Michael Larsen, MD, DMSc, Inger C. Munch, MD, PhD, Steffen Hamann, MD, PhD Background: Optic disc drusen (ODD) are seen in up to 2.4% of the general population, but the etiology and pathophysiology of the condition is still unknown. The purpose of this study was to determine the prevalence of ODD in a population-based child cohort and to determine if scleral canal diameter and fetal birth and pubertal parameters are associated with the presence of ODD. Methods: This observational, longitudinal population-based birth cohort study, with a nested case-control, included 1,406 children. Eye examinations were performed when the children were between 11 and 12 years of age. Assessment was performed of optical coherence tomography (OCT) scans from 1,304 children with gradable enhanced depth imaging scans of the optic disc. Results: ODD in one or both eyes were found in 13 (1.0%) of all children. All but one of the cases were found in children with scleral canal diameter in the lowest quartile (1,182- 1,399 mm) in the nested case-control study. Children with ODD had a mean disc diameter of 1,339 mm (interquartile range, 30 mm), whereas it was 1,508 mm (interquartile range, 196 mm) in the 130 controls without ODD (P , 0.001). No differences in sex, birth weight, refractive error, and Tanner stages (of puberty) were found between children with and without ODD. Conclusions: The prevalence of ODD was 1% in a large child cohort examined by OCT. ODD was found only in eyes with a narrow scleral canal, which is consistent with the hypothesis that ODD might arise as a conse- Department of Ophthalmology (LM, XQL, CLE, ML, SH), Rigshospitalet, University of Copenhagen, Glostrup, Denmark; Faculty of Health and Medical Sciences (LM, ML, ICM, SH), University of Copenhagen, Copenhagen, Denmark; Department of Public Health (AMS, EMO), Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark; National Institute of Public Health (AMS), Faculty of Health Sciences, University of Southern Denmark, Odense, Denmark; and Department of Ophthalmology (ICM), Zealand University Hospital, Roskilde, Denmark. Supported by Jørgen Bagenkop Nielsens Myopi-Fond, Øjenforeningen, Fight for Sight Denmark, and Synoptik-Fonden. The authors report no conflicts of interest. Address correspondence to Lasse Malmqvist, MD, Department of Ophthalmology, Rigshospitalet, Nordre Ringvej 57, 2600 Glostrup, Denmark; E-mail: lasse.malmqvist.larsen.01@regionh.dk 140 quence of retinal nerve fiber congestion in the scleral canal. Journal of Neuro-Ophthalmology 2018;38:140-146 doi: 10.1097/WNO.0000000000000567 © 2017 by North American Neuro-Ophthalmology Society O ptic disc drusen (ODD) have a reported prevalence in adults of 0.2%-3.1% (1-3). The lower prevalence of 0.37% reported in children (4) suggests that ODD expand and become more visible with age (5). The pathophysiology of ODD is still unknown and several theories have been proposed. Tso (6) theorized that disturbances in axonal metabolism would lead to extrusion of mitochondria that later calcify (6). A more recent hypotheses is that a small scleral canal causes a compression of the axons in the optic nerve head, which leads to extrusion of axonal material, such as mitochondria, RNA, DNA, and iron (3,7-9). Conflicting results about scleral canal size have questioned the latter theory (10,11). Adults with large drusen can have peripapillary retinal nerve fiber layer (RNFL) deficits and visual field defects (12-14). Such defects are rarely seen in children with ODD (15-17). Ophthalmoscopy, ultrasonography, and autofluorescence fundus photography have been the main modalities for identifying ODD. Optical coherence tomography (OCT) is an attractive nonmydriatic, non-contact alternative. With a depth penetration up to half a millimeter behind the retinal pigment epithelium (18) and an axial resolution of 7 mm, enhanced depth imaging OCT (EDI-OCT) is capable of detecting small, deeply located ODD and has been found to have a higher ODD detection rate than other methods (19). The aim of our study was to examine the prevalence of ODD and the association between ODD and scleral canal diameter in preadolescent children. Using EDI-OCT we were able to evaluate a large representative population cohort of 1,406 children to detect buried ODD. Malmqvist et al: J Neuro-Ophthalmol 2018; 38: 140-146 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution METHODS Study Population The Copenhagen Child Cohort Eye Study examined children at the age of 11-12 years in 2011-2012. The eye examination was part of the larger study "the Copenhagen Child Cohort 2000" also involving core mental health examinations (20). The study was approved by the Scientific Ethics Committee of the Capital Region of Denmark and performed in accordance with the Helsinki Declaration. Informed consent was obtained from the children's parents or legal guardians before the examinations. Data Acquisition Collection of data was performed as previously described (21). Briefly, participants were questioned about ophthalmic and medical history and medication use. Best-corrected visual acuity was determined using Early Treatment Diabetic Retinopathy Study charts (4 m original series; Precision-Vision, La Salle, IL). Ocular axial length was measured using an interferometric device (IOL-MASTER, version 3.01.0294; Carl Zeiss Meditec, La Jolla, CA). Subjective refraction was performed guided by objective refractioning (Retinomax K-plus 2; Right MFG. CO, LTD, Tokyo, Japan). Fundus photography was obtained nondilated (Topcon Retinal Camera MW6S; Topcon Medical Systems, Oakland, NJ). Spectral-domain OCT (Spectralis HRA+OCT; Heidelberg Engineering, Heidelberg, Germany) was made in enhanced-depth imaging mode with the following scanning procedures: a 20° 6-line radial scan of the optic disc used for ODD screening, a 12° peripapillary circumferential scan used to measure RNFL thickness, and a 30° transfoveal 7-line horizontal scan used to measure subfoveal choroidal thickness (22). All scans were performed in high resolution with averaging of 25 B-scans using the built-in eye tracking feature. Image Analysis OCT scans were analyzed using the manufacturer's software (Heidelberg Eye Explorer, version 1.6.1.0; Heidelberg Engineering). Transverse magnification was estimated as previously described (23). An experienced grader (L.M.) assessed all OCT scans (n = 2634). ODD were identified as circumscribed hyporeflective spheroidal elements located in front of the lamina cribrosa, fully or partially surrounded by a hyperreflective border (Fig. 1A, B). The presence of ODD was identified by an experienced grader (L.M.) and confirmed by an expert in neuro-ophthalmology (S.H.). Eleven children were excluded from the study as they were classified as having technically correct but anatomically ungradable scans. All these 11 children had pseudopapilledema with hyperreflective bands in front of the lamina cribrosa that did not meet the criteria of ODD (Fig. 1C, D). Mean scleral canal diameter was measured in all children with ODD and in 10 times as many controls consisting of randomly selected children from the cohort without ODD. All children included in the nested case-control analysis were white. The mean scleral canal diameter was assessed by identifying the edge of Bruch membrane on opposing side FIG. 1. Enhanced depth imaging optical coherence tomography scans of optic nerve heads. A and B. Optic disc drusen (arrows) characterized by a round cross section, a uniformly hyporeflective center, and a thin hyperreflective margin. Arrowheads indicate retinal vessels, which cast a typical shadow. C and D. Hyperreflective bands (dotted arrows) at different depths within the optic nerve head primarily are found close to the lamina cribrosa. Malmqvist et al: J Neuro-Ophthalmol 2018; 38: 140-146 141 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 2. A. The scleral canal diameter is measured as the mean of 6 radial enhanced depth imaging optical coherence tomography scans. Arrow illustrates tomography orientation of the scan on the right-hand side. B. The scleral canal is defined as the Bruch membrane opening measured from the termination of Bruch membrane on opposing sides (arrows). This measure is equivalent to the inner aspects of the scleral canal opening (horizontal line). of the optic disc in the 6 radial disc-centered OCT scans. This measure was equivalent to the inner aspects of the scleral canal opening (Fig. 2). Intraobserver and interobserver variability (L.M., C.L.E.) was assessed in 30 randomly selected children and examined using Bland-Altman plots. Intraobserver variability was calculated from repeated measurements made at 3-month intervals. The mean intraobserver difference for scleral canal diameter was 12.7 mm (SD ± 9.7 mm) without trend or bias. The mean interobserver difference was 21.3 mm (SD ± 15.3 mm), also without trend or bias. Fundus photographs were only analyzed in children with ODD and exclusively for the occurrence of visible (superficial) ODD. The racial distribution of the children was obtained using the self-reported parental country of birth. The pubertal development was self-assessed according to the Tanner classification with gender-specific standard reference drawings depicting pubic hair, breast size and form, and other characteristics (24,25). Maternal tobacco consumption during pregnancy was classified as follows: did not smoke, ceased smoking, or continued smoking. Information about gestational age, birth weight, and self-reported maternal smoking (tobacco) during pregnancy was retrieved from the Danish Medical Birth Registry, which includes pregnancy, birth, and infant data reported by midwifes and obstetricians in Denmark. Statistics Statistical analyses were performed using SAS statistical software (SAS 9.4; SAS Institute, Cacy, NC). Mean values and SDs or medians and interquartile ranges (IQRs) (skewed distributions) were calculated for continuous variables. The scleral canal diameter was calculated as the mean of the 6 measurements per eye. Mean scleral canal diameter was also used to calculate the 142 scleral canal area for comparison with earlier literature. Spherical equivalent refraction was calculated as the algebraic sum of the value of the sphere and half the cylinder. In children without ODD, only the right eye was used for the analyses. In children with bilateral ODD, the eye with subjectively estimated largest volume of ODD was used. In children with unilateral ODD, only the affected eye was assessed. We used Student t test or Wilcoxon signed rank test (skewed distribution) to compare the group of children with ODD with the group of children without ODD. Chi-square/Fisher exact tests were used for categorical data. In the analysis of scleral canal diameter characteristics, cases of ODD were compared with the controls in the nested case-control study. The relation between RNFL thickness and scleral canal diameter was tested in a linear regression model. We used histograms and Kolmogorov- Smirnov test to ensure assumptions of normal distribution and homogeneity of variance. The assumptions of linearity, variance homogeneity, and normality of the distribution of residuals underlying the linear regression model were assessed by review of relevant plots. The level of statistical significance for comparisons was set at P , 0.05. RESULTS The Copenhagen Child Cohort Eye Study included examination of 1,406 children. A total of 1,304 participants were eligible for the present analysis. The 102 exclusions were made because of inability to obtain high quality optical coherence tomography scans (n = 13), absence of an optic disc scan (n = 32), ungradable scans (n = 11) and poor patient cooperation at the eye examination (n = 35) or at the axial length measurement (n = 11) used to estimate transverse magnification. Both eyes were examined in all children. Of the 1,304 included children, 13 were found to have ODD in at least one eye, corresponding to Malmqvist et al: J Neuro-Ophthalmol 2018; 38: 140-146 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution TABLE 1. Characteristics of 11- to 12-year-old children with and without optic disc drusen Number (%) Boys/girls, % Age (IQR), yr Visual acuity, ETDRS letters Refractive error, D Axial length (IQR), mm Tanner pubertal development stage, n (%) 1 2 3 4 Birth weight, g Gestational age at birth (IQR), d Maternal smoking during pregnancy, n (%) None Ceased smoking Continued smoking Mean RNFL thickness (IQR), mm Subfoveal choroidal thickness (IQR), mm Scleral canal diameter (IQR), mm Optic Disc Drusen No Drusen Controls Without Drusen 13 (1%) 46/54 11.4 (0.7) 90.1 ± 2.8 0.01 ± 0.49 22.9 (0.68) 1291 (99%) 48/52 11.6 (0.7) 88.8 ± 3.3 0.09 ± 0.93 23.2 (1.0) 130 (10%) 42/58 11.4 (0.5) 89.6 ± 2.9 20.02 ± 0.54 23.1 (1.2) 3 (23.1%) 8 (61.5%) 2 (15.4%) 0 (0%) 3589 ± 359 283 (9) 272 (22.1%) 651 (52.8%) 278 (22.6%) 31 (2.5%) 3544 ± 597 280 (13) 33 (26.2%) 69 (54.8%) 23 (18.3%) 1 (0.8%) 3581 ± 639 282 (11) 10 (76.9%) 1 (7.7%) 2 (15.4%) 105 (10) 411 (71) 1339 (30) 1024 (81%) 23 (1.8%) 217 (17.2%) 104 (12) 356 (104) - 107 (83.6%) 3 (2.3%) 18 (14.1%) 104 (14) 362 (87) 1508 (196) P value* 0.92† 0.95‡ 0.15§ 0.58§ 0.12‡ 0.91† 0.66§ 0.13‡ 0.27† 0.44‡ 0.028‡ ,0.001‡ Data are presented as mean ± SD or as proportions. In variables with skewed distribution, median and interquartile range are presented. *P-values represent comparisons between children with optic disc drusen and all children without drusen, except for scleral canal diameter where the comparison was between children with optic disc drusen and a random subsample of 130 children without drusen. † 2 x test. ‡ Wilcoxon rank sum test. § Student t test. d, days; D, diopters; ETDRS, Early Treatment Diabetic Retinopathy Study; g, grams; IQR, interquartile range; RNFL, retinal nerve fiber layer. a per-person prevalence of 1.0% (Table 1). Eight children had bilateral ODD and 2 children had drusen that were visible on fundus photographs. The children with ODD had a median scleral canal diameter of 1,339 mm (IQR, 30 mm) and the nested controls had a median scleral canal diameter of 1,508 mm (IQR, 196 mm), P , 0.0001 (Table 1). All but one child with ODD had a scleral canal diameter in the lowest quartile of the children in the nested control group, P , 0.001 (Table 2 and Fig. 3). The scleral canal in the average eye with ODD was 21% smaller than in the average control eye (1.41 vs 1.79 mm2). Mean RNFL thickness was not significantly different between the 2 groups (Table 1), and no correlation between RNFL thickness and scleral canal diameter was found (P = 0.64) (Fig. 3). Children with ODD had a thicker subfoveal choroid with a mean thickness of 411 mm (IQR, 71 mm) compared with 356 mm (IQR, 104 mm) for children in the cohort without ODD (P = 0.028, Table 1). There were no significant differences between children with and without ODD in birth weight, gestational age at birth, sex, or maternal tobacco consumption during pregnancy, and there was no difference at the time of examination, in age, refractive error, axial length, visual acuity, or pubertal development (Table 1). All children included in the nested case-control analysis were white. DISCUSSION In this cross-sectional study of 1,304 children, we found a prevalence of ODD of 1.0% using EDI-OCT. To the best of our knowledge, only a single, smaller, clinic-based study has previously examined the prevalence of ODD, TABLE 2. Optic disc drusen and scleral canal diameter quartiles in the nested case-control study Mean Scleral Canal Diameter in Quartiles Controls (n) Optic disc drusen children, n Total Q1 1,182-1,399 mm Q2 1,400-1,500 mm Q3 1,501-1,605 mm Q4 1,606-2,034 mm Total 23 12 35 35 1 36 36 0 36 36 0 36 130 13 143 Malmqvist et al: J Neuro-Ophthalmol 2018; 38: 140-146 143 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 3. Peripapillary mean retinal nerve fiber layer thickness (RNFL) in relation to mean scleral canal diameter in 11- to 12year-old children, including 13 children with optic disc drusen (black circles) and a nested control group of 130 children without optic disc drusen (open circles). which were visible in children (4). In that study, an ODD prevalence of 0.4% in a Finnish child cohort was found using slit-lamp ophthalmoscopy, a method that is clearly less sensitive than OCT. The children had a mean age of 9.4 years compared to 11.4 years in our study. If ODD in this study had been diagnosed only using fundus photography, the resulting prevalence had been only 0.15%. In cadaver eyes, a prevalence of 2.4% was found, supporting the fact that a large fraction of ODD is not visible by slitlamp ophthalmoscopy (2). The prevalence of 1.0% found in the present study using EDI-OCT is comparable to the 0.2%-3.1% values found in adult populations using previous methods of diagnosing ODD (1-3). The present study may have underestimated the prevalence of ODD because we excluded 11 children with prelaminar hyperreflective bands on OCT. If hyperreflective bands happen to be an early sign of ODD, or conglomerates of small ODD, then the total ODD and presumptive ODD precursor lesions in our cohort would rise to 1.8%. The hyperreflective bands could, however, represent artifacts or, when deeply located, the anterior border of the lamina cribrosa. Prospective studies will likely provide more information about the utility of OCT as method of diagnosing disc drusen, and follow-up on this group of children are planned in a future study. It has been suggested that developmental or environmental factors might play a role in the etiology of ODD due to its irregular autosomal pattern of inheritance (1). In the present study, no significant differences in perinatal and pubertal parameters were found between children with and without ODD. An ancillary finding of our report was that the subfoveal choroid was thicker in children with ODD than in those 144 without ODD. There was no correlation between scleral canal diameter and choroidal thickness or axial length in the nested controls, suggesting that this ancillary finding may be mere coincidence. When performing Bonferroni adjustment, the difference in choroidal thickness between the groups was insignificant (P = 0.34). Several OCT studies, exclusively in adults, found thin RNFL in eyes with visible ODD (13,14,16,26,27). We found no such association in children, and we suspect that nerve fiber layer attenuation is associated only with ODD that have had time to extend to such dimensions that they damage the nerve fibers in the optic nerve head (12). With a mean age of 11.6 years, the ODD might not have had the time to do enough axonal damage to be reflected in RNFL thickness or the ODD might still be immature and flexible, leaving axons undamaged. We found that the mean scleral canal diameter in eyes with ODD was below the 25% percentile in 92% of children with ODD, which supports the hypothesis that ODD might develop as the result of nerve fiber compression in a narrow scleral canal. In 1978, Spencer (28) proposed that the formation of ODD is caused by compromised axonal transport in a narrow scleral canal. Fundus photography studies have found smaller scleral canals in ODD eyes than in control eyes (8,9). However, OCT studies have produced conflicting results by finding larger scleral canals in ODD eyes compared to control eyes (10,11). A major difference between the 2 methods is that delineation of the scleral canal depends on the visibility of the edge of the retinal pigment epithelium on fundus photography, whereas the scleral canal is defined by the Bruch membrane opening on OCT. This often results in a smaller diameter with the latter method. Additionally, large ODD may extend beyond the margins of the scleral canal and Malmqvist et al: J Neuro-Ophthalmol 2018; 38: 140-146 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution displace the surrounding structures and lead to overestimation of the scleral canal diameter (10). Masking from overlying ODD and even from the protruding optic disc might also cause larger scleral canal measures. This is supported by a study that found larger scleral canals in eyes with superficial ODD than in eyes with buried ODD (15). The younger age and earlier stage of ODD development in our study population eliminates this masking and displacement problem. The scleral canals in our healthy children were of the same size (mean 1.86 mm2) as adult control subjects examined by Floyd et al (10) (mean 1.83 mm2) and by Flores-Rodríguez et al (11) (1.66-1.76 mm2). This further supports that masking from overlying ODD, and displacement of Bruch membrane opening could be the cause of contradicting results in the literature. Another explanation for the conflicting results in scleral canal size could be that eyes with ODD start out with small scleral canals, but then enlarge in adulthood. To the best of our knowledge, OCT follow-up studies on scleral canal size have been performed in neither eye-healthy individuals nor patients with ODD. Longitudinal OCT studies focusing on optic nerve head morphology are needed. Not every small disc had ODD. Obviously, a narrow scleral canal may not be the only risk factor for ODD. However, we suspect that among unidentified risk factors, there may be other aspects of nerve fiber compression in the optic nerve head, such as localized "hotspots" of nerve fiber congestion in the lamina cribrosa. Despite a large number of children in the cohort, the main limitation of our study was the small proportion of children with ODD. The radial scans were ideal for measuring scleral canal diameter but ODD might have been overlooked in some children with limited morphological changes. The use of autofluorescence and B-scan ultrasound could have been valuable in these cases. Solely diagnosing ODD using EDIOCT might be a limitation. However, EDI-OCT has been found to have a higher ODD detection rate than other diagnostic methods (19) and might soon be acknowledged as "gold standard" in ODD diagnostics. There also could be falsepositive cases in this study, but it is based on previous studies of ODD that used all currently available methods of diagnosing ODD (19,29-31). The formula for calculating scleral canal area assumes that the optic disc is a regular circle, which is not the case. Different methods have been used for area calculations in other studies. Hence, this measure was only used for literature comparison and not used in the statistical analyses. The results of this study suggest an association between a small scleral canal and ODD, which is consistent with the hypothesis that ODD might arise as a consequence of nerve fiber congestion in the scleral canal. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: L. Malmqvist, X. Q. Li, A. M. Skovgaard, E. M. Olsen, M. Larsen, I. C. Munch, and S. Hamann; b. Acquisition of data: L. Malmqvist, X. Q. Li, A. M. Skovgaard, E. M. Malmqvist et al: J Neuro-Ophthalmol 2018; 38: 140-146 Olsen, and M. Larsen; c. Analysis and interpretation of data: L. Malmqvist, X. Q. Li, C. L. Eckmann, A. M. Skovgaard, E. M. Olsen, M. Larsen, I. C. Munch, and S. Hamann. Category 2: a. Drafting the manuscript: L. Malmqvist; b. Revising it for intellectual content: L. Malmqvist, X. Q. Li, C. L. Eckmann, A. M. Skovgaard, E. M. Olsen, M. Larsen, I. C. Munch, and S. Hamann. Category 3: a. 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Date | 2018-06 |
Language | eng |
Format | application/pdf |
Type | Text |
Publication Type | Journal Article |
Source | Journal of Neuro-Ophthalmology, June 2018, Volume 38, Issue 2 |
Publisher | Lippincott, Williams & Wilkins |
Holding Institution | Spencer S. Eccles Health Sciences Library, University of Utah, 10 N 1900 E SLC, UT 84112-5890 |
Rights Management | © North American Neuro-Ophthalmology Society |
ARK | ark:/87278/s6hx5zzh |
Setname | ehsl_novel_jno |
ID | 1452574 |
Reference URL | https://collections.lib.utah.edu/ark:/87278/s6hx5zzh |