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ORIGINAL ARTICLE
Year : 2019  |  Volume : 67  |  Issue : 6  |  Page : 788-794

Ultra-widefield fundus fluorescein angiography in pediatric retinal vascular diseases


Dr Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi, India

Date of Submission08-Oct-2018
Date of Acceptance26-Apr-2019
Date of Web Publication24-May-2019

Correspondence Address:
Dr. Shreyas Temkar
Dr Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, Ansari Nagar, New Delhi - 110 029
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijo.IJO_1688_18

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  Abstract 


Purpose: To describe the utility of RetCam ultra-wide-field fundus fluorescein angiography in pediatric retinal vascular diseases. Methods: A retrospective chart review was carried out in 43 eyes of 22 pediatric patients who were diagnosed or suspected to have a retinal vascular disease. Fluorescein angiography was carried out using the 130 degree lens of RetCam 3. Fluorescein angiography guided treatment (laser/cryotherapy) was carried out wherever required. Results: Diseases studied included - coats disease, familial exudative vitreoretinopathy, retinopathy of prematurity, congenital retinal folds, double optic nerve head, persistent fetal vasculature and incontinentia pigmenti. RetCam assisted fluorescein angiography was helpful in establishing a diagnosis in 4 patients (18%), in decision making regarding treatment in 18 patients (82%), in deciding need for retreatment in 5 patients (23%), helped in staging of disease in 5 patients (23%) and in detecting clinically subtle findings in 6 patients (27%). Conclusion: RetCam assisted FFA is extremely useful to document peripheral retinal vascular pathologies in pediatric patients and helps to take crucial therapeutic and retreatment decisions.

Keywords: Fluorescein angiography, RetCam, retinal vascular diseases, retinopathy of prematurity, widefield imaging


How to cite this article:
Temkar S, Azad SV, Chawla R, Damodaran S, Garg G, Regani H, Nawazish S, Raj N, Venkatraman V. Ultra-widefield fundus fluorescein angiography in pediatric retinal vascular diseases. Indian J Ophthalmol 2019;67:788-94

How to cite this URL:
Temkar S, Azad SV, Chawla R, Damodaran S, Garg G, Regani H, Nawazish S, Raj N, Venkatraman V. Ultra-widefield fundus fluorescein angiography in pediatric retinal vascular diseases. Indian J Ophthalmol [serial online] 2019 [cited 2019 Jun 26];67:788-94. Available from: http://www.ijo.in/text.asp?2019/67/6/788/259022



A large subset of pediatric vitreoretinal disorders is due to pathologies of the retinal vasculature. Vascular disorders of children include conditions like retinopathy of prematurity (ROP), familial exudative vitreoretinopathy (FEVR), Coats disease, persistent fetal vasculature, incontinentia pigmenti, Norrie disease and vasculitis.[1] Most of these disorders present with peripheral retinal vascular abnormalities. A proper assessment of many of these cases requires an examination under anesthesia. Additionally, these disorders can be better studied by fluorescein angiography. It is difficult to perform conventional fluorescein angiography in children as it requires good patient cooperation. Also, the field of view with most fundus cameras is limited; hence, the assessment and documentation of peripheral fundus abnormalities is met with difficulty.[2] Various modalities of widefield imaging have been described in children.[3],[4],[5],[6] RetCam (Clarity Medical Systems, Inc.) is a widefield contact imaging device specifically developed for use in pediatric population. The latest version, RetCam 3, has option for fluorescein angiography and has been shown to be a useful tool for imaging vasculature in pediatric patients.[7],[8],[9],[10],[11],[12] This study was conducted to further assess the utility of RetCam fluorescein angiography in patients with different types of pediatric vascular disorders.


  Methods Top


This was a retrospective chart review carried out in 43 eyes of 22 pediatric patients in whom conventional fundus imaging and fluorescein angiography was not possible or in whom additional procedures like laser or cryotherapy were planned as a part of the management. The study was conducted at Dr Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences. Patients were recruited from the retina and retinopathy of prematurity services of the hospital. The study adhered to the tenets of Declaration of Helsinki. Written informed consent was taken for performing RetCam imaging, fluorescein angiography, and expected interventions like laser or cryotherapy. Clearance from pediatrician was obtained in all small babies and patients with suspected systemic illness. RetCam imaging was carried out either under pediatrician monitoring (in babies <3 months) or under general anesthesia (in bigger children). Fundus photography (FP) and fundus fluorescein angiography (FFA) was done using RetCam 130° widefield lens. Intravenous sodium fluorescein (20%) was injected at a dose of 0.04 ml/kg or 7.7 mg/kg followed by an immediate saline flush.[13],[14] Fluorescein angiography-guided treatment (laser/cryotherapy) was carried out wherever required. Follow-up visits were planned based on disease type, severity, and decision of the surgeon.


  Results Top


RetCam-guided imaging and FFA was carried out in 43 eyes of 22 patients. 15 cases were male and 7 were females. Their age ranged from 4 weeks to 10 years. We studied 6 cases of Coats disease, 5 cases of FEVR, 5 cases of ROP, 3 cases of congenital retinal folds, 1 case of double optic nerve head, 1 case of persistent fetal vasculature, and 1 case of incontinentia pigmenti. [Table 1] summarizes the details of patients and the disease entities included in the study.
Table 1: Demographic details of patients and the disease entities included in the study (RE - right eye, LE - left eye, BE - both eyes, APROP - aggressive posterior retinopathy of prematurity, FEVR - familial exudative vitreoretinopathy)

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Of the 5 cases of Coats disease, 4 were males and 1 was a female patient. All cases were unilateral. FFA revealed telangiectatic and aneurysmal changes and areas of avascular retina. No evidence of significant vascular abnormalities was noted in the fellow eye of any patient. RetCam-assisted FFA was helpful to confirm the diagnosis, detect capillary nonperfusion areas and areas of vascular anomaly which required laser/cryotherapy. Additional follow-up RetCam fluorescein angiography of these cases was helpful in deciding adequacy of therapy/need for augmentation of therapy [Figure 1], [Figure 2],[Figure 3].
Figure 1: (a-d) A 5-year-old male patient with Coats disease. Right eye shows extensive lipid exudation (a), corresponding FFA image shows presence of numerous aneurysmal and telangiectactic changes along with capillary drop out areas in temporal retina (c, black arrows). No evidence of vascular abnormalities was noted in the fellow eye (b and d)

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Figure 2: (a-f) A 1.5-year-old female patient who presented with leucocoria in the left eye. There was bullous retinal detachment with some peripheral vascular abnormalities in the left eye (a and b). FFA revealed presence of extensive telangiectasia and aneurysmal changes (d and e, black arrows). FFA of the right eye did not reveal any vascular abnormality (f). Diagnosis of Coats disease was confirmed in this case based on the FFA findings

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Figure 3: (a-d) A 6-year-old male child, diagnosed case of left eye Coats disease (previously cryotherapy treated). Right eye had a parafoveal lipid plaque and temporal cryotherapy scars (a, asterisk). FFA revealed parafoveal staining corresponding to the lipid plaque (b). Peripheral scans revealed the presence of localized area of telangiectasia and aneurysmal changes in the superior retina suggestive of residual activity (c, encircled area). Laser therapy was carried out selectively to this area. Right eye did not reveal any vascular abnormalities (d)

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All cases of FEVR had bilateral disease. Out of 10 eyes, 2 eyes had close funnel RD (stage 5), 5 eyes had stage 1, 2 eyes had stage 2, and 1 eye had stage 3 disease. RetCam-assisted FFA was useful in staging of the disease, to know the extent of avascular areas (for treatment), and to know the need for retreatment during follow-up [Figure 4] and [Figure 5].
Figure 4: (a-d) A 2-year-old female patient with stage 1 FEVR. RetCam FFA in this case was useful to stage the disease, to know the extent of retinal avascularity (white arrows) and to rule out neovascularization

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Figure 5: (a-d) A 3-year-old male patient with stage 2 FEVR with extensive retinal neovascularization in left eye (a and b). Right eye had close funnel retinal detachment. 8 weeks post laser fundus photo (c) and corresponding FFA image showing persistent small capillary dropout area (white arrows) with residual fine neovascularization (asterisk). Laser augmentation was done in this case

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Of the total 10 eyes of ROP, 6 eyes had aggressive posterior ROP and 4 eyes had ROP sequelae. In case of APROP, RetCam-assisted FFA was extremely useful to identify the extent of retinal vascularization, to identify avascular loops, and to know the status of macular perfusion [Figure 6].
Figure 6: (a-f) A 29 weeks born preterm child examined at 33 weeks postconceptional age. Fundus examination (a and b) showed presence of ill-defined posterior pole disease (Zone 1 APROP). RetCam FFA revealed only part of zone 1 to be vascularized with incomplete vascularization of the macula (white arrows). Multiple avascular loops can also be noted (c and d). Intravitreal anti-VEGF therapy was planned in both eyes. At 4 weeks post-injection, macula appeared vascularized with retinal vasculature extending upto zone 2 (e and f)

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In 2 patients with ROP sequelae, 1 eye of each patient had a total retinal detachment. The other eye of the first patient was found to have avascular retina in Zone 3 and in the second patient a floating venous loop was identified.[15]

Out of the 3 cases of congenital retinal folds, two cases had a family history of FEVR [Figure 7]. In one patient, the cause of retinal fold was attributed to ROP. In these cases, RetCam FFA assisted in making a final diagnosis and ruling out any persistent disease activity.
Figure 7: (a-h) A 3-year-old male child presenting with low vision and nystagmus. Both eyes had tractional retinal folds (a and b, white asterisks). The cause of these retinal folds was not certain. RetCam FFA revealed bilateral vascularized retinal folds (c and d, black asterisks). RetCam assisted FFA of 1.5-year-old (e and f) and 5-year- old (g and h) siblings showing features typical of FEVR

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One patient had clinical anophthalmos in one eye and evidence of double optic nerve head in the other eye. FFA clearly demonstrated evidence of two independent retinal circulations arising from each of the optic nerve heads [Figure 8]. FFA could detect bilateral temporal avascular retina in one case of incontinentia pigmenti. One case had unilateral posterior persistent fetal vasculature with a stellate fibrous membrane over disc with radiating folds. FFA showed staining of the membrane with absence of any peripheral vascular abnormalities.
Figure 8: (a and b) A 4 weeks old female presenting with RE anophthalmos and LE congenital corneal opacity (a inset). Fundus examination of the left eye revealed evidence of double optic nerve head (a). The second optic nerve was colobomatous (white arrow). Retcam FFA confirmed the presence of double retinal circulation in the left eye arising from the two optic nerve heads

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Complications and difficulties encountered

None of the patients in the study developed anesthesia complications or allergic reactions to fluorescein injection like rash, respiratory distress, tachycardia, fever, and local injection site reactions. In 1 patient of APROP, who had extensive iris neovascularization, imaging of the late phases was met with difficulty due to leakage of the dye into the anterior chamber obscuring the fundus details.

Treatment

Fluorescein angiography assisted laser treatment by Laser Indirect Ophthalmoscopy was carried out in 23 eyes immediately after performing angiography. Direct visualization of the FFA images on the RetCam screen helped the surgeon to precisely identify and treat the vascular abnormalities and avascular retina. In cases where the posterior segment neovascularization was extensive, the dye leaking into vitreous cavity caused a slight greenish haze but laser treatment could be successfully achieved in all cases.

Twelve patients received laser for the treatment of vascular abnormalities. One patient received cryotherapy. Three patients received retreatment with laser based on persistence of disease/avascular retina on FFA on follow-up. One eye received retreatment with cryotherapy.

In our study performing a RetCam assisted fluorescein angiography in addition to the clinical assessment helped in establishing a diagnosis in 4 patients (18%). The diagnosis of Coats was established in 1 case and FEVR was diagnosed in 3 cases. This technique helped in decision making regarding treatment in 18 patients (82%), and in deciding need for retreatment in 5 patients (23%). It helped in staging the disease in (FEVR, Coats and ROP) 5 patients (23%) and detecting clinically subtle findings in (e.g. small NVE, venous loop) in 6 patients (27%). Presence of two independent vascular arcades emanating from two disc-like structures helped in confirming a very rare diagnosis of double optic nerve head in 1 patient (5%). [Table 2] summarizes the advantages gained by use of RetCam widefield fluorescein angiography over clinical findings and it's influence in changing management plan [Table 2].
Table 2: Advantages gained by use of RetCam widefield fluorescein angiography over clinical findings

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  Discussion Top


The purpose of this study was to evaluate the utility of RetCam FFA in the management of pediatric retinal vascular disorders. In this study, we intended to see if FFA would provide more details compared only to clinical examination or imaging only. RetCam-assisted FFA not only was able to confirm and corroborate with the clinical findings but also provided excellent details of the fundus pathology not appreciated on color photography alone.

Treatment in most of the adult retinal vascular diseases is guided by fluorescein angiography. Since conventional FFA including the Spectralis and Optos require patient cooperation, RetCam serves as an excellent tool to image the pediatric patients not comfortable with the conventional imaging.

In our retrospective study, a wide range of pediatric retinal vascular disorders were included. RetCam FFA enabled in establishing a diagnosis in 18% cases and defining treatment in 82% cases as discussed in detail in the results.

We did FFA only in selected cases of APROP where there was clinical confusion to decide management. In one of our cases, FFA helped to identify incomplete macular perfusion and hence was decided to carry out injection intravitreal anti-VEGF over laser procedure. Follow-up of this case showed vascularization progressing upto anterior zone 2. Also in 2 cases, FFA helped to identify all the areas of avascular loops. Identification and laser of these loops is essential for complete regression of the disease. Studies have also shown that FFA can be useful to detect vascular and macular abnormalities seen in cases of ROP and in eyes treated with intravitreal Bevacizumab.[16],[17] Also, FFA images appear to be easier to interpret than RetCam images, in cases of ROP with a high degree of reliability, even where trainee practitioners are involved.[18]

RetCam FFA was extremely useful in a female child with exudative detachment to make a diagnosis of Coats disease with certainty by revealing characteristic telangiectasia and capillary nonperfusion areas which could not be easily picked up clinically. The utility of FFA in a similar case has been reported previously by Koozekanani et al.[11] In other cases of Coats disease, FFA was useful for identification of areas requiring treatment, to guide in retreatment by identifying residual areas of avascularity and neovascularization. FFA guided treatment in early stages of Coats has been shown to result in good anatomic and visual outcomes by providing valuable information not provided by clinical examination alone.[12] In our series, widefield FFA using RetCam was extremely convenient to screen the fellow eyes. The occurrence of angiographic vascular abnormalities in a clinically normal appearing fellow eye has been shown in various studies.[19],[20] Thus, it is preferable to thoroughly screen clinically normal appearing fellow eyes of Coats disease to look for subtle angiographic signs.

In cases of FEVR, manifestations range from asymptomatic disease to total retinal detachment. RetCam FFA in our patients was mainly useful to decide the need for treatment and retreatment. FFA helps to clearly identify variety of vascular abnormalities, which are not picked by clinical examination. It has also been noted previously that vascular leakage without clinical exudation can be detected only by angiography and early treatment before exudation is critical for favorable outcomes.[21]

Congenital retinal fold is a condition characterized by a vascular retinal fold extending from optic disc towards peripheral fundus. These folds are thought to result from insufficient retinal vascular development in conditions like FEVR, ROP, Norrie disease, and incontinentia pigmenti.[22] Unlike cases of persistent fetal vasculature, these cases tend to be bilateral. In our series, the cause of these folds could be attributable to FEVR and ROP.

Other few interesting pathologies picked up in our series of cases were a floating venous loop causing vitreous hemorrhage (the details of this case have been published in the same journal)[15] and double optic nerve head. True double optic nerve head is a rare entity. Similar to the previous reports on true double optic nerve head,[23] our case had two independent retinal circulations arising from the two discs. However, we could not carry out MRI and other imaging modalities as the parents denied for further investigations.

The study has a few limitations. This was a retrospective study with a variable duration of follow-up. Also, we did not do a direct comparison between clinical examination based treatment and FFA guided treatment.


  Conclusion Top


RetCam-assisted FFA is an extremely useful investigation in the management of pediatric retinal vascular diseases. Widefield angiographic images help to analyze and document subtle peripheral vascular pathologies that can be missed on clinical examination. RetCam FFA guides the surgeon in making crucial therapeutic and retreatment decisions.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Feiner L, Prenner JL. Retinal Vascular Disease in Children. Available from: https://www.reviewofophthalmology.com/article/retinal-vascular-disease-in-children. [Published 2016 Apr 12].  Back to cited text no. 1
    
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Nagiel A, Lalane RA, Sadda SR, Schwartz SD. Ultra-widefield fundus imaging: A review of clinical applications and future trends. Retina Phila Pa 2016;36:660-78.  Back to cited text no. 2
    
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Magnusdottir V, Vehmeijer WB, Eliasdottir TS, Hardarson SH, Schalij-Delfos NE, Stefánsson E. Fundus imaging in newborn children with wide-field scanning laser ophthalmoscope. Acta Ophthalmol (Copenh) 2017;95:842-4.  Back to cited text no. 3
    
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Kang KB, Wessel MM, Tong J, D'Amico DJ, Chan RV. Ultra-widefield imaging for the management of pediatric retinal diseases. J Pediatr Ophthalmol Strabismus 2013;50:282-8.  Back to cited text no. 4
    
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Fung THM, Yusuf IH, Xue K, Smith LM, Patel CK. Heidelberg spectralis ultra-widefield fundus fluorescein angiography in infants. Am J Ophthalmol 2015;159:78-84.e1-2.  Back to cited text no. 5
    
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Fung THM, Muqit MMK, Mordant DJ, Smith LM, Patel CK. Noncontact high-resolution ultra-wide-field oral fluorescein angiography in premature infants with retinopathy of prematurity. JAMA Ophthalmol 2014;132:108-10.  Back to cited text no. 6
    
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Azad R, Chandra P, Khan MA, Darswal A. Role of intravenous fluorescein angiography in early detection and regression of retinopathy of prematurity. J Pediatr Ophthalmol Strabismus 2008;45:36-9.  Back to cited text no. 7
    
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Wu C, Petersen RA, VanderVeen DK. RetCam imaging for retinopathy of prematurity screening. J AAPOS 2006;10:107-11.  Back to cited text no. 8
    
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Purcaro V, Velia P, Baldascino A, Antonio B, Papacci P, Patrizia P, et al. Fluorescein angiography and retinal vascular development in premature infants. J Matern-Fetal Neonatal Med 2012;25(Suppl 3):53-6.  Back to cited text no. 9
    
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Escudero J, Borras F, Fernández MA, Domínguez C. [Fluorescein angiography with RetCam in incontinentia pigmenti: A case report]. Arch Soc Espanola Oftalmol 2009;84:529-32.  Back to cited text no. 10
    
11.
Koozekanani DD, Connor TB, Wirostko WJ. RetCam II fluorescein angiography to guide treatment and diagnosis of coats disease. Ophthalmic Surg Lasers Imaging 2010:1-3. doi: 10.3928/15428877-20100215-86.  Back to cited text no. 11
    
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Suzani M, Moore AT. Intraoperative fluorescein angiography-guided treatment in children with early Coats' disease. Ophthalmology 2015;122:1195-202.  Back to cited text no. 12
    
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Hartne ME. Pediatric Retina. Lippincott Williams and Wilkins, Philadelphia; 2005.  Back to cited text no. 13
    
14.
Luxme Hariharan, Rachitskaya R, Hess DJ, Rodriquez A, Negron C, Berrocal A. Serial fundus photography and fluorescein angiography after off-label intravitreal bevacizumab treatment for retinopathy of prematurity: Importance of monitoring regression by angiography in off-label bevacizumab treated eyes. JAAPOS 2014;18:e4.  Back to cited text no. 14
    
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Temkar S, Damodaran S, Chawla R, Behera S, Bafna RK, Parmanand K. Floating venous loop in regressed retinopathy of prematurity. Indian J Ophthalmol 2018;66:568-9.  Back to cited text no. 15
[PUBMED]  [Full text]  
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Zepeda-Romero LC, Oregon-Miranda AA, Lizarraga-Barrón DS, Gutiérrez-Camarena O, Meza-Anguiano A, Gutiérrez-Padilla JA. Early retinopathy of prematurity findings identified with fluorescein angiography. Graefes Arch Clin Exp Ophthalmol 2013;251:2093-7.  Back to cited text no. 16
    
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Lepore D, Molle F, Pagliara MM, Baldascino A, Angora C, Sammartino M, et al. Atlas of fluorescein angiographic findings in eyes undergoing laser for retinopathy of prematurity. Ophthalmology 2011;118:168-75.  Back to cited text no. 17
    
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Guagliano R, Barillà D, Bertone C, Maffia A, Periti F, Spallone L, et al. Fluorescein angiography-based diagnosis for retinopathy of prematurity: Expert-non expert comparison. Eur J Ophthalmol 2013;23:881-6.  Back to cited text no. 18
    
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Jung EH, Kim JH, Kim SJ, Yu YS. Fluorescein angiographic abnormalities in the contralateral eye with normal fundus in children with unilateral Coats' disease. Korean J Ophthalmol 2018;32:65-9.  Back to cited text no. 19
    
20.
Blair MP, Ulrich JN, Elizabeth Hartnett M, Shapiro MJ. Peripheral retinal nonperfusion in fellow eyes in coats disease. Retina Phila Pa 2013;33:1694-9.  Back to cited text no. 20
    
21.
Kashani AH, Brown KT, Chang E, Drenser KA, Capone A, Trese MT. Diversity of retinal vascular anomalies in patients with familial exudative vitreoretinopathy. Ophthalmology 2014;121:2220-7.  Back to cited text no. 21
    
22.
Nishina S, Suzuki Y, Yokoi T, Kobayashi Y, Noda E, Azuma N. Clinical features of congenital retinal folds. Am J Ophthalmol 2012;153:81-7.e1.  Back to cited text no. 22
    
23.
Padhi TR, Samal B, Kesarwani S, Basu S, Das T. Optic disc doubling. J Neuro-Ophthalmol 2012;32:238-9.  Back to cited text no. 23
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]
 
 
    Tables

  [Table 1], [Table 2]



 

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