Background: Ultra-widefield angiography is the latest technology in the evolution of fundus fluorescein angiog- raphy. With the ability to capture up to 200° of the fundus in a single image, far peripheral retinal pathology can be imaged. Generally, obtaining high-quality fundus fluorescein angiography in a child without sedation in the outpa- tient setting is exceedingly challenging. Therefore, there are advantages to imaging platforms that can capture the peripheral retina in young children without anesthesia. Often pediatric retinal diseases have pathology localized to the far periphery, which further validates the utility of ultra-widefield angiography. Ultra-widefield angiography has been successfully used without sedation for evaluation of children with various pediatric retinal diseases such as Coats disease, familial exudative vitreoretinopathy, and retinopathy of prematurity. Conclusion: This non-contact, non-mydriatic modality has been utilized in the evaluation of pediatric retinal diseases and demonstrated to have benefits over conventional fluorescein angiography techniques. Keywords: Ultra-widefield fluorescein angiography, Ultra-wide field imaging, Pediatric retina, Coats disease, Familial exudative vitreoretinopathy, Retinopathy of prematurity, Incontentia pigmenti Background neovascularization obtained by fluorescein angiography For nearly six decades, fluorescein angiography has been are paramount to the management of proliferative and a diagnostic staple in the diagnosis and management of exudative pediatric retinal diseases. Therefore, there has vitreoretinal diseases, graphically demonstrating infor- been an evolution of imaging modalities to better capture mation regarding circulations of the retina, choroid and the peripheral retina with fluorescein angiography. optic nerve head, and barrier integrity of the neurosen- Techniques were developed to create montages of sory retina and retina pigment epithelium. Capturing images from several fields captured by fundus photogra - quality angiographic images of the peripheral retina with phy to widen the field of view capable with standard 30 or a 30°–60° field of view of most standard fundus cameras 50 degree cameras. The 7 Standard Fields (7SF) protocol proved difficult [ 1]. This requires a skilled photographer for fundus photography was developed and popularized and a cooperative patient able to maintain steady gaze by the Diabetic Retinopathy Study group expanded visu- in various directions. This challenge is particularly true alization to approximately 75° with 3 photos horizontally when imaging pediatric patients. Retinal diseases affect - across the macula and 4 photos surrounding the optic ing the pediatric population include a number of genetic disc . Similarly, a 9 Standard Fields protocol was used and environmentally influenced conditions that involve in monitoring cytomegalovirus retinitis . However, the peripheral retina, including as examples, retinopathy the time sensitive nature of fluorescein angiography in of prematurity (ROP), familial exudative vitreoretinopa- addition to the technical difficulty capturing images by thy (FEVR) and Coats disease [2–4]. Information regard- photography to create montages made such a technique ing the perfusion of the retina, vascular leakage, and cumbersome and still often left large areas of peripheral retina not visualized. This technique was very difficult in children or infants. *Correspondence: email@example.com Widefield angiography, capturing > 30° to < 200° , John A. Moran Eye Center, University of Utah, 65 Mario Capecchi Dr., Salt was developed as a solution to the limitations of standard Lake City, UT 84132, USA © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Calvo and Hartnett Int J Retin Vitr (2018) 4:21 Page 2 of 6 angiography with traditional fundus cameras. The Stau - the limitations of the Optos platform are the distortion renghi contact lens system (Ocular Staurenghi 230 SLO and decreased resolution of the far periphery as well as Retina Lens; Ocular Instruments Inc, Bellevue, WA, reduced superior and inferior fundus imaging in com- USA) achieved imaging up to 150° with a standard con- parison to the temporal and nasal fundus . More focal scanning laser ophthalmoscope . The contact recently, Heidelberg (Heidelberg Engineering, Germany) lens requires patient cooperation because of the direct released their noncontact lens system that attaches to the corneal contact which is a challenge for adult patients Heidelberg Spectralis and Retina Angiograph platforms but particularly difficulty for most pediatric patients. The to achieve ultra-widefield photography and angiography Pomerantzeff Equator-Plus camera  and the Panoret) . CMT Medical Technologies Inc, Valley Stream, NY(  visualized 148° and 130° of the retina, respectively; how- Pediatric conditions imaged with ultra‑widefield ever, their popularity was limited by the need for mydria- angiography sis, contact lenses, and that both systems are stand-alone As discussed above, in the pediatric population, imag- instruments that cannot be integrated with existing ing of the peripheral retinal often required general anes- fundus cameras. The Retcam (Clarity Medical Systems, thesia. Initially, standard 30° or 45° cameras were used Pleasanton, California, USA) portable contact-based and required positioning of the eye to the periphery in camera, now in its third generation, with a 130° field of children who were unable to cooperate. Contact cam- view entered the market in 1997 and made its niche in eras were helpful but also required general anesthesia. pediatric ophthalmology and pediatric retina . The However, with UWFA, there is the ability to obtain qual- portability of the Retcam allowed for bedside and operat- ity images in some children without the need for gen- ing room imaging of pediatric patients and the handheld eral anesthesia. We describe several conditions below in contact camera allowed for manual rotation of globe in which UWFA has provided adequate images for diagno- very young patients or those under anesthesia. Infants sis and treatment without the need for general anesthe- can undergo imaging with Retcam in the office with sia. The PubMed database was systematically searched swaddling, lid speculum, and topical anesthesia but older using the search terms [(pediatric or pediatric retina or children most commonly require general anesthesia. Coats or familiar exudative retinopathy) and (fluores - The Optos camera (Optos 200Tx, Dunfermline, Scot - cein angiography or widefield imaging or ultra-widefield land, UK) was the first ultra-widefield imaging system, imaging)]. To our knowledge, all articles or abstracts which produces a 200° view of the retina (about 82% describing the use of ultra-widefield fluorescein angiog - of the surface area) [12, 13]. In addition, the Optomap raphy in the pediatric population were included in this auto-montage software can image 220° or about 97% of review (Table 1). the retina. A confocal scanning laser ophthalmoscope is combined with an ellipsoidal mirror to image the retinal Familial exudative vitreoretinopathy periphery with one capture without the need for a con- Familial exudative vitreoretinopathy (FEVR) has a vari- tact lens, and most often, without mydriasis. Some of able presentation, including straightened retinal vessels, Table 1 Summary of UWFA reports Author # of patients Patient ages Diagnoses Notable conclusions Kang et al. 8 9, 10, 10, 11, 11, 14, 14, 14 FEVR, Coats A significant degree of pathology was outside of 7 Standard Fields overlay Tsui et al. 16 5, 5, 6, 6, 7, 8, 8, 9, 10, 11, Coats, pars planitis X-linked retinoschisis, Eyelash artifact was present in 12 of 40 images 11, 12, 12, 12, 12, 12 retinal dystrophy, choroidal melanoma, (30%) juvenile idiopathic arthritis, toxoplasmosis, panuveitis Rabiolo et al. 5 8, 8, 12, 13, 15 Coats 77.8% of unaffected eyes had peripheral abnormalities such as nonperfusion and telangiectasia Patel et al. 1 3 months old Incontentia pigmenti ‘Flying baby’ technique was used to position the child. Oral 2% fluorescein solution was safely used Fung et al. 3 Infant born at 27 weeks ROP ‘Flying baby’ technique used; NICU team pre- sent to monitor child in this position Infant born at 24 weeks Infant born at 29 weeks Calvo and Hartnett Int J Retin Vitr (2018) 4:21 Page 3 of 6 temporal dragging of the macula, abnormal retinal vas- Table 2 Revised familial exudative vitreoretinopathy clinical staging system  cular permeability (Fig. 1), described as late-phase angi- ographic posterior and peripheral vascular leakage Stage Description (LAPPEL), and capillary/vascular non-perfusion, which 1 Avascular periphery or anomalous intraretinal vascularization may be a consequence of leaky retinal vessels. Capil- 1a Without exudate or leakage lary nonperfusion can progress toward the macula and 1b With exudate or leakage threaten vision or be associated with later intravitreal 2 Avascular retinal periphery with extraretinal vascularization neovascularization, which can lead to complex tractional 2a Without exudate or leakage retinal detachments. Both increased permeability and 2b With exudate or leakage vitreous traction from intravitreal neovascularization can 3 Extramacular retinal detachment lead to vision loss and blindness . 3a Without exudate or leakage In FEVR, myopia is present and family history should 3b With exudate or leakage be sought as genetic mutations are recognized in about 4 Macula-involving retinal detachment 50% of cases, but the condition is variable in expressivity 4a Without exudate or leakage so even a normal parent may pass onto offspring a muta - 4b With exudate or leakage tion manifesting as disease. Many of the early findings 5 Total retinal detachment of FEVR occur in the far peripheral retina making the 5a Open funnel diagnosis challenging. The findings are best appreciated 5b Closed funnel with fluorescein angiography that demonstrates capillary non-perfusion and leakage of the vascular front in the region between vascularized and avascular retina. There treatment session of laser photocoagulation. Kang et al. is also intravitreal neovascularization in Stage 2 FEVR concluded that standard 7SF fluorescein angiography (Table 2) that shows exuberant leakage in late stages. would not have identified these areas of pathology. There UWFA permits good visualization of the nasal and tem- were no reported complications or loss of vision. poral peripheral retinas even in some children. In a series of five patients ranging from 11 to 14 years of age, ultra- widefield fundus photography and ultra-widefield fluo - Coats disease rescein angiography were used to successfully capture Coats disease presents with symptoms in one eye usu- angiographic images in all . Laser photocoagulation ally and is more common in boys than in girls (~ 80 vs. was performed in 2 eyes of 2 patients with UWFA guid- 20%). Contact Retcam imaging has identified periph - ing treatment to target areas of peripheral non-perfusion. eral areas of nonperfused retina in the fellow eye of Repeated UWFA allowed for identification of regions patients with Coats disease, which is more than three of untreated non-perfusion and guided the second standard deviations greater than the < 1 disc diameter of Fig. 1 Representative photo of ultra-widefield angiography of two children with familial exudative vitreoretinopathy. a Right eye of a 9 year old child with persistent retinal nonperfusion posterior to prior laser photocoagulation. b Left eye of a 10 year old child with prominent temporal vascular dragging, hyperfluorescence and leakage from neovascularization Calvo and Hartnett Int J Retin Vitr (2018) 4:21 Page 4 of 6 the borders of the 7 Standard Fields. UWFA-guided laser photocoagulation resulted in reduction in exudation, resolution of leaking telangiectatic vessels, and decreased macular edema demonstrated by repeat UWFA. Tsui et al. demonstrated the outpatient use of UWFA without sedation in younger children, aged 6 and 7 years old, with Coats disease . Targeted laser photocoagulation was also performed. In a report by Rabiolo et al., five children and teenagers (ages 8–15) received UWFA imaging in an outpatient setting . Only 1 child was treatment naïve with all other patients having been previously treated with laser photocoagulation or cryotherapy. In addition to concluding that UWFA captured more peripheral reti- nal pathology than standard FA, the authors determined by UWFA that 77.8% of asymptomatic fellow eyes had far Fig. 2 Representative photo of ultra-widefield angiography in an 8 year old child with Coats disease. Laser photocoagulation was peripheral nonperfusion and capillary telangiectasias. performed previously to telangiectatic vessels and there is staining of chronic exudation in the superior macula Incontentia pigmenti Incontinentia pigmenti is an inherited X-linked dominant disease, mainly seen in females as it is lethal in males. Table 3 Coats disease staging classification  Avascular retina is seen and vessels can develop and Stage Description remodel normally but if intravitreal neovascularization occurs, there is a risk of vision loss from vitreous hem- 1 Retinal telangiectasia only orrhage and tractional retinal detachment. Vision loss 2 Telangiectasia and exudates also occurs from avascularity in the macula . Laser 2a Extrafoveal exudation treatment can cause regression of neovascularization and 2b Foveal exudation reduce the risk of later retinal detachment. Fluorescein 3 Exudative retinal detachment angiography is useful to diagnose non-perfused retina 3a Subtotal retinal detachment (1) extrafoveal (2) foveal and leakage of fluorescein from intravitreal neovasculari - 3b Total retinal detachment zaiton, but the condition manifests in infancy often, and 4 Total retinal detachment and glaucoma imaging requires general anesthesia for early diagnosis 5 Advanced end-stage disease and management. There is a single report demonstrating the application of UWFA for the evaluation of inconten- tia pigmenti . A 3 month old infant girl underwent UWFA in an outpatient office setting. Oral fluorescein non-pathologic, nonperfused, temporal retina in normal, 2% solution was given at a dose of 25 mg/kg via a bottle young children . Other vascular abnormalities such with a mixture of infant formula milk 30 min prior. No as telangiectasias and microaneurysms can be found sedation was provided. Following standard pupillary dila- in the fellow eyes of patients with Coats but these are tion and placement of a lid speculum, the child was held often asymptomatic . When bilateral symptomatic in a ‘flying baby’ position with the body and head sup - Coats disease does occur, it can be in association with ported and the technician aligning the infant’s eye with fascioscapular muscular dystrophy. Treatment of Coats the lens. In under 5 min, successful angiography was per- disease is often with laser directly to abnormal telangi- formed with images of the far periphery in all quadrants. ectatic vasculature and scatter treatment to the attached Retinal ischemia, arteriovenous shunting, and neovascu- nonperfused retinal areas in early stages of Coats disease larization were well documented. There were no reported (Fig. 2; Table 3). In stages 3 and 4 Coats disease, external complications from the oral fluorescein or the position - drainage of subretinal fluid sometimes in combination ing of the child. with vitrectomy and silicone oil are used. UWFA has been extensively utilized in the evaluation and management of Coats disease [17, 19, 20]. Three chil - Retinopathy of prematurity dren with the diagnosis of Coats disease ranging from 9 Retinopathy of prematurity (ROP) is a leading cause of to 14 years of age underwent UWFA. In an overlay of 7 blindness and vision loss worldwide in premature infants. Standard Fields protocol to UWFA images, all areas of ROP is identified by screening infants at risk and moni - retinal telangiectasia and non-perfusion were outside of toring until physiologic vascularization has extended to Calvo and Hartnett Int J Retin Vitr (2018) 4:21 Page 5 of 6 the ora serrata. Type I ROP is treated with laser photo- cognitive development [30–32]. Additionally, in-office coagulation or intravitreal anti-VEGF agents. In the past, UWFA is likely to be less stressful for the child’s family fluorescein angiography was not standard care for ROP and less time-consuming for all parties involved. [23, 24]. However, with the advent of agents that inhibit However, there are definite limitations of UWFA. the bioactivity of vascular endothelial growth factor Poor image quality, distortion, and artifact may affect up (VEGF) and studies that test efficacy and safety of dose, to 5–10% of images in some studies [33, 34]. Naturally, it has been realized that anti-VEGF agents can change this distortion is related to the two-dimensional repre- the natural history of ROP and that intravitreal neovas- sentation of the rounded, three-dimensional surface of cularization and later tractional retinal detachments the fundus. However, a method for rectifying peripheral occur even a year after an injection . Fluorescein distortions when calculating retinal area and measuring angiography has increasingly been used to understand lesions has been described . Inferior eyelash artifact the pathophysiologic course of ROP following intravit- was present in 12 of 40 images (30%) in one study . real anti-VEGF agents [26–28]. In the only report of the The Optos platform does not image the far superior and use of UWFA in infants with retinopathy of prematurity inferior peripheral retina as extensively as compared with (ROP), Fung and colleagues published a consecutive case its imaging of the temporal and nasal retina . The series of 3 infants with ROP born 24–29 weeks gestation Heidelberg Spectralis was shown to image the superior that underwent UWFA in an outpatient office setting and inferior retinal vasculature more peripherally than . UWFA was performed with the ‘flying baby’ tech - the Optos Optomap in nine of ten eyes (18 of 20 quad- nique supporting the head and baby so the eye could be rants); however, the Optos Optomap could image the imaged following administration of oral fluorescein and nasal and temporal retinal vasculature more peripherally without any sedation. Of note, a neonatal intensive care in ten of ten eyes (20 of 20 quadrants) . Though dem - team was present for monitoring of the child during the onstrated to be used successfully in three infants with procedure. High-resolution angiograms were obtained ROP and one infant with incontinentia pigmenti, it may in 3 of 3 infants and no complications were reported, not be safe to routinely image such children in the office however, the authors noted the prone, ‘flying baby’ could with the required precarious positioning. result in cardiopulmonary complications in these medi- Ultra-widefield angiography is a valuable adjunct to cally-fragile infants. The authors concluded that UWFA traditional forms of fluorescein angiography as the tech - allowed for imaging significantly more of the peripheral nique proves to be less invasive and better tolerated in retina in a single image than the 130° fundus imaging of pediatric patients. The greater ability of UWFA to iden - the Retcam camera. tify peripheral retinal pathology over conventional angi- ography platforms is especially suited to pediatric retinal conditions such as Coats disease and FEVR. The future Miscellaneous will hold better and less invasive methods of imaging the UWFA has also been successfully used in the evaluation peripheral retina vasculature such as ultra-widefield opti - of children with X-linked retinoschisis, Stargardt disease, cal coherence tomography (OCT) angiography . Fur- Best’s disease, toxoplasmosis chorioretinitis, juvenile sar- ther studies utilizing UWFA are warranted to integrate coidosis, choroidal melanoma, juvenile idiopathic arthri- UWFA into management recommendations for pediatric tis, pars planitis, and traumatic retinal detachment . retinal conditions. Ages ranged from 5 to 12 years old. Conclusions Abbreviations UWFA: ultra-widefield fluorescein angiography; ROP: retinopathy of prematu- Ultra-widefield fluorescein angiography has established rity; FEVR: familial exudative vitreoretinopathy; 7SF: 7 Standard Fields. itself as a useful tool to the vitreoretinal specialist and is proving to be valuable in the care of pediatric retina Authors’ contributions CC performed the review of literature, collected images and was the major patients. There is mounting evidence that UWFA may be contributor in writing the manuscript. Both authors read and approved the a valuable adjunct to identify peripheral retinal pathology final manuscript. undetected by the conventional 75° field from 7 Stand - ard Fields in the evaluation of pediatric retinal diseases Acknowledgements . There is a clear benefit in avoiding examinations None. under anesthesia for those children who may be able to Competing interests cooperate with noncontact angiography. Repeated gen- The authors declare that they have no competing interests. eral anesthesia may pose a significant cardiopulmonary risk to systemically ill children. There have been concerns Availability of data and materials Not applicable. raised about the effect of repeated general anesthesia on Calvo and Hartnett Int J Retin Vitr (2018) 4:21 Page 6 of 6 Consent for publication 19. Tsui I, Franco-Cardenas V, Hubschman J-P, Schwartz SD. Pediatric retinal Not applicable. conditions imaged by ultra wide field fluorescein angiography. 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Published: Jun 5, 2018