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(SUNDROP): Five Years of Screening with Telemedicine

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■ CLINICAL SCIENCE ■ Stanford University Network for Diagnosis of Retinopathy of Prematurity (SUNDROP): Five Years of Screening With Telemedicine Natalia Fijalkowski, BA; Luo Luo Zheng, BS; Michael T. Henderson, BA; Sean K. Wang, BS; Matthew B. Wallenstein, MD; Theodore Leng, MD, MS; Darius M. Moshfeghi, MD INTRODUCTION BACKGROUND AND OBJECTIVE: To report the 5-year results of the Stanford University Network for Diag- Retinopathy of prematurity (ROP) is a vision- nosis of Retinopathy of Prematurity (SUNDROP) tele- threatening disease of disordered retinal vasculature medicine initiative. development in premature and low birth weight in- fants.1,2 The underdeveloped retina overcompensates PATIENTS AND METHODS: Infants requiring retinopathy for ischemia at birth by promoting angiogenesis that of prematurity (ROP) screening at six neonatal inten- can damage nearby structures through retinal edema, sive care units from December 1, 2005, to November traction, or detachment.3,4 At United States schools, 30, 2010, were evaluated with remote retinal photogra- ROP accounts for 14% of pediatric blindness.5 The phy by an ROP specialist. Every infant received outpa- World Health Organization (WHO) found ROP to be tient binocular indirect ophthalmoscope examinations the leading cause of avoidable visual impairment in until termination criteria were achieved or until treat- high-income countries and the second leading cause ment. Outcomes were treatment-warranted ROP (TW- in middle-income countries,6 accounting for 15% to ROP, ETROP type 1) and adverse anatomical events. 35% of pediatric blindness in some nations.7-9 Randomized trials and observational studies RESULTS: Five hundred eleven infants (1,022 eyes) were demonstrate that cryotherapy,10,11 laser photocoagu- screened. Fifteen infants had TW-ROP and underwent lation,12-15 and intravitreal bevacizumab16,17 can pre- laser photocoagulation. The TW-ROP cohort had sig- serve vision when administered early in the course nificantly lower birth weight and gestational age (both of disease.14 Armed with vision-saving treatments, P < .001). No patient progressed to adverse anatomical public health efforts have shifted toward screening outcomes and no case of TW-ROP was missed. Tele- and promptly identifying high-risk infants. The land- medicine had 100% sensitivity, 99.8% specificity, mark Early Treatment of Retinopathy of Prematurity 93.8% positive predictive value, and 100% negative (ETROP) trial developed standardized screening time predictive value for detection of TW-ROP. lines based on the natural course of ROP and defined the criteria for initiation of treatment (ETROP type CONCLUSION: Telemedicine demonstrates high di- 1).4,14 In 2013, the American Academy of Pediatrics agnostic accuracy for detection of TW-ROP and can (AAP) and the American Academy of Ophthalmology complement ROP screening. (AAO) released updated ROP screening recommenda- tions stating that every infant with birth weight less [Ophthalmic Surg Lasers Imaging Retina. 2014;45:106-113.] than or equal to 1,500 g, estimated gestational age From the Byers Eye Institute, Horngren Family Vitreoretinal Center, Department of Ophthalmology, Stanford University School of Medicine, Palo Alto, California (NF, LLZ, MTH, SKW, TL, DMM); and the Lucile Packard Children’s Hospital, Department of Pediatrics, Stanford University School of Medicine, Palo Alto, California (MBW). Originally submitted May 21, 2013. Accepted for publication October 23, 2013. Posted online January 20, 2014. Supported by the National Institutes of Health (NIH) Clinical and Translational Science Awards (CTSA) offered through the Stanford Center for Clinical Informatics (CTSA award number UL1 RR025744). Ms. Fijalkowski was supported by the NIH CTSA in Epidemiology and Biostatistics offered through the Stanford School of Medicine Center for Clinical and Translational Research Education (CTSA award number UL1 TR000093). The authors have no financial or proprietary interest in the materials presented herein. Dr. Moshfeghi did not participate in the editorial review of this manuscript. The authors would like to acknowledge Dr. Kristin Sainani, professor of statistics and epidemiology at the Stanford University Health Services and Research Policy Department, for her editorial expertise and assistance with revision as well as inspiring their team to effectively communicate their science through good writing. Address correspondence to Darius M. Moshfeghi, MD, Byers Eye Institute, Horngren Family Vitreoretinal Center, Dept. of Ophthalmology, Stanford Univer- sity School of Medicine, 2452 Watson Court, Room 2277, Palo Alto, CA 94303; 650-644-5561; fax: 650-565-8297; Skype: dmoshfeghi. doi: 10.3928/23258160-20140122-01 106 Ophthalmic Surgery, Lasers & Imaging Retina | Healio.com/OSLIRetina Figure. Images in each eye were external (top left), optic nerve (ON) centered, ON superior, ON inferior (bottom left), ON nasal, and ON temporal. Figure is reproduced with permission from Graefe’s Archive for Clinical and Experimental Ophthalmology. less than or equal to 30 weeks, or an unstable clinical in one location and transmit them to a remote expert course deemed high risk by the attending pediatrician for interpretation. Telemedicine, the use of electronic should be screened with serial eye examinations until technology for remote health care, is promising for the infant meets criteria for terminating screening.18 ROP screening because it may serve as a cost-effective Although screening and treatment are highly effective complement to traditional bedside binocular indirect at preventing ROP related vision loss, thousands of ophthalmoscope (BIO) examination performed by the at-risk infants worldwide remain unscreened because ophthalmologist.21 Among studies comparing tele- of a shortage of ROP specialists.19 medicine with concurrent BIO for detection of treat- The number of neonates requiring screening is ment-warranted ROP, all have found high diagnostic increasing because sophisticated neonatal intensive accuracy.22-28 Most importantly, no infant in any pub- care unit (NICU) technology enables the survival of lished telemedicine study with disease necessitating younger infants worldwide. At the same time, the intervention has been missed. number of physicians willing and able to care for The Stanford University Network for the Diagno- these patients is dwindling. Pediatric ophthalmolo- sis of Retinopathy of Prematurity (SUNDROP) is an gists are already at a shortage in the United States,8 active community initiative that uses telemedicine as and a survey by the AAO projects a 17% decline the sole in-hospital screening technique for high-risk in the current ROP workforce due to legal liability, infants born at six satellite NICUs located through- travel burden, poor reimbursement, and significant out Northern California. The SUNDROP initiative time commitments.20 These shortages are amplified was developed to reduce blindness and poor visual in middle-income countries where there are fewer outcomes from ROP by providing infants in rural practicing pediatric ophthalmologists.19 and county hospitals with quaternary care. The SUN- The ROP screening burden may be alleviated with DROP initiative is the first true implementation of the use of wide-angle digital retinal photography in- telemedicine for ROP screening in the United States. terpreted remotely to complement the work of pediat- All infants meeting AAP/AAO criteria are screened ric ophthalmologists and retina specialists. The ROP with RetCam II images that are sent to the Stanford screening examination relies upon visual analysis of University Byers Eye Institute reading center for re- anatomic structures that can be seen in a photograph. mote interpretation by an ROP specialist, and out- Retinal image devices such as the RetCam II (Clarity comes are confirmed with outpatient ophthalmology Medical Systems, Pleasanton, CA) are now able to follow-up. This report summarizes the 5-year results capture high-resolution digital images from patients of the SUNDROP initiative. March/April 2014 · Vol. 45, No. 2 107 NICUs are located throughout Northern TABLE 1 California and include level I, II, and Comparison of Baseline Characteristics of Infants With III nurseries encompassing community, and Without Treatment-Warranted Retinopathy of private, and county hospitals. Thus, the Prematurity in the SUNDROP Telemedicine Initiative screened infants are a demographically, ethnically, and socioeconomically di- Patient TW-ROP (n = 15), No TW-ROP (n = 496), verse population. This study includes Characteristic Mean ± SD Mean ± SD infants screened from December 1, Gender 2005, to November 30, 2010. The birth Male (%) 66.7 54.9 weight was obtained from the delivery record and further classified into cat- Female (%) 33.3 45.1 egories of extremely low birth weight Estimated gestational 24.8 ± 1.7 29.0 ± 2.8 (less than 1,000 g), very low birth age (weeks)* weight (1,000-1,499 g) and low birth Birth weight (grams)* 678.2 ± 148.5 1,275.0 ± 347.5 weight (1,500-2,500 g) consistent with Multiplicity** WHO classifications. Gender, estimated Single (%) 73.3 84.7 gestational age, and multiplicity data were also obtained from the delivery re- Twin (%) 26.7 14.1 cords at each hospital. Births were clas- Triplet (%) 0.0 1.2 sified as single, twin (including both Number of exams* 10.3 ± 5.8 3.3 ± 2.9 dizygotic and monozygotic), or triplet. Number of images* 144.7 ± 47.5 40.5 ± 44.8 Photography Protocol Adverse outcomes¥ 0 0 NICU nurses were trained to take
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