Retinopathy of prematurity (ROP) is a leading cause of childhood blindness the world-over. ROP is a disease of the retina that affects preterm, low birth weight infants and has the potential to cause permanent and irreversible blindness, fortunately which is largely preventable.
Retinopathy of prematurity is a major public health problem. India, like other middle-income countries is experiencing the ‘third epidemic’ of blindness due to ROP and is the country with the highest number of preterm births i.e. 3.5 million annually. Of the 27 million live-births, approximately 9% are born below 2000 grams, the potential ‘at-risk’ population for ROP. However, there are considerable challenges to controlling ROP in India, on account of the increasing provision of neonatal intensive care services with improving neonatal survival, lack of quality neonatal services, lack of awareness even among care-givers, and inadequately trained man-power for screening and treating ROP, most of whom are located in the large cities. An additional factor is that heavier, more mature infants are also at risk of severe ROP in middle-income countries, including India, which increases the number to be screened. We have recently reported that ROP also affects infants cared for in smaller, rural locations, exploding the myth that it is restricted to tertiary care urban centers. A region-specific strategy is required which addresses these complexities, and an on-going endeavor in India is summarized in this manuscript.
K.I.D.R.O.P. - Karnataka Internet Assisted Diagnosis of Retinopathy of Pre-maturity was initiated in 2007 to address the problems of unscreened rural and semi-urban premature infants for ROP, using a novel platform of telemedicine and employing for the first time, non-physician graders who travel to remote neonatal intensive care units (NICUs). They use a portable wide-field retinal digital camera (Retcam Shuttle, Clarity MSI, CA, USA) to take retinal images which they grade and interpret and make management decisions while in the NICU (i.e. discharge; screen again and when; urgent referral to an ophthalmologist required). Images captured by the graders are also uploaded and read on the smart phones of ROP specialists in the city or elsewhere on a customized ‘Tele-ROP app’ and platform (iPhone app, “iCare-TeleOphthalmology” i2i Tele-solutions, Bangalore, India).
This manuscript presents a comprehensive report of several aspects of the program including the working methodology, validation results of technicians to diagnose and decide follow-up, a score for technician training and accreditation, validating smart phone reporting for ROP images and summarizes the lessons learnt in the past six years.
Materials and Methods
K.I.D.R.O.P. currently provides ROP screening for 81 neonatal intensive care units (NICU's) across 18 districts of Karnataka State in Southern India. There are 3 dedicated teams (‘Team A's’) and 12 ‘Team B’s’ for 12 of the district headquarters who were trained and validated in Bangalore. The program was initiated by Narayana Nethralaya Postgraduate Institute of Ophthalmology (NNPIO), Bangalore as a stand-alone program, initially as a pilot for 6 districts in 2008. The NNPIO has undertaken all the training and validation studies.
The program has expanded as a ‘public private partnership’ under the aegis of the National Rural Health Mission, Ministry of Health and Family Welfare, Government of Karnataka (since 2009). All images, data and reports analyzed in this manuscript are restricted to the 6 districts not covered under the PPP and owned by NNPIO. The Institution Review Board, the Research Committee and the Ethics Committee of NNPIO have approved this program.
Team composition and role
A ‘Team A’ comprises a project manager, one or two trained and validated technician (s), a driver and a vehicle. Each team is equipped with a Retcam Shuttle (Clarity MSI, USA), a portable laser (532nm green) with laser indirect ophthalmoscopy (LIO) delivery, a laptop with data connectivity, Tele-Care software (i2i Telesolutions, Bangalore, India) and consumables. Each team travels on a fixed schedule on a weekly time-table, visiting the same NICU at a fixed time on a fixed day each week within a radius of approximately 300 kms from their respective headquarters. Overnight accommodation is arranged at the headquarters or adjoining districts depending on the distance and logistics. On an average, 1200-1600 kms are travelled each week and an average of 16-28 NICU's visited by a single team weekly. Besides these scheduled centers, there are NICU's who have a smaller case load and are visited on an ‘on-call’ basis. The project manager's responsibilities include scheduling infants, reminding mothers, recording and analyzing data obtained during imaging sessions. We have evolved a novel, low-cost method of recruiting infants from centers where the team does not routinely visit. The manager also plays a vital role of being the liaison between the ROP expert and the neonatologist or pediatrician, the resident doctors, nurses and mothers, especially in promoting recruitment and reducing follow-up attrition. ‘B teams’ are from the local districts, trained by KIDROP and are not the subject of this manuscript.
At each session, technicians perform a modified PHOTO-ROP group imaging sequence to include 7 (minimum) images per eye i.e. dilated anterior segment (obtained without any lens by inverting the Retcam camera). The other six images are obtained using the 130°(ROP lens) provided by the manufacturer and include - macula center, disc center, temporal, superior, nasal and inferior quadrants. Additional images of pathology are obtained at the discretion of the technician. All images are captured in video mode and relevant stills are saved in the database. All images are obtained in the NICU, the step down room or the eye office under topical anesthesia (Proparacain, 0.5%) complying with standard guidelines.
Training, validation and accreditation of technicians: (The “STAT” score)
Training and validating a technician is germane to the KIDROP program. We have evolved a training methodology with a scoring system, which we use to accredit a novice technician through levels of expertise [Table 1]. This has resulted from the collective experience of training several private and government teams and is called the “KIDROP STAT” (S core for T raining and A ccreditation of T echnicians) and comprises 3 levels (Level I, II and III) in a 20 point score. The scored parameters include basic knowledge of the disease and the program (1-3), imaging related (4-13), which scores the ability of the technician to obtain well focused, oriented images in a proper sequence which includes the temporal ora or at least zone 3, and speed of acquisition. Image grading and reporting (14-16) relate to his or her ability to diagnose and make a clinical management decision. Decision triage is performed using a template created by KIDROP and includes a 3-way triage using images from both eyes [Table 2]: RED - (Type 1 ROP or serious disease in one or both eyes probably needing treatment or at least urgent evaluation by the expert), ORANGE (Type 2 ROP in at least one eye where follow up is needed; and GREEN (can be discharged). Post imaging (17-19) parameters test the ability of the technician to upload the images, use the Tele-Care software, record the details and aid the project manager in scheduling subsequent follow-up visits using images to educate the mothers. The last parameter on the score is management of complications (20) and is assessed for level II and III technicians.
The ‘levels’ in the STAT score are created to be water-tight compartments rather than an ‘across-the-board’ point system used in other scoring systems. This ensures stricter entry criteria into each level, necessitating all tasks to be completed before accreditation. For example, to qualify as level I, simply having good knowledge of the program and data management will not suffice, if the technician possesses poor skill of image capture or grading and vice-versa. Furthermore, as the expertise increases, speed must improve (6 minutes to 2 minutes per eye), grading scores must improve (60 to > 90%), and the number of routine uploads must decrease from all images to only RED's. This ensures that once a technician reaches Level III, he or she is required to upload only images of RED infants, so that the decision of referral can be verified by an expert. Objective scores are obtained for parameters described in 5,6712 16 and 19. Other parameters are assessed using pre and post-tests, theory and practical ‘live’ assessments. In our program it takes approximately 30 working days to ‘create’ a Level I and 90 days for a Level III technician. Trainees progress from observation and practicing on a mannequin (Retcam Imaging Practice Kit (Clarity MSI, USA) to live sessions first under supervision and then independently until they are adept in image acquisition and decision making.
Software and smart phones
Images obtained during the session are also uploaded using the TeleCare Software (i2i Telesolutions and Telemedicine Pvt. Ltd, Bangalore). This uploading template is installed on another laptop (non Retcam laptop) with internet connectivity via a USB Data card. Images are transferred from the Retcam laptop onto this device using a new CD each time or through a wired LAN connection. Technicians upload images on this customized platform. The software employs patented lossless technology, which is agnostic to the format of the incoming image (MLX, DICOM, PNG or JPEG), allowing universality. The priority of upload is Red > Orange > Green which depends on the level of the technician [Tables 1 and 2]. Increasing expertise would shift it to the left. Following upload, images are available on a virtual work list for the remote expert to read and report. The reporting template uses the International Classification of Retinopathy of Prematurity (ICROP) classification and Early Treatment for Retinopathy of Prematurity (ETROP) grade for treatment in a ‘drop-down menu’ for rapid ‘click’. On submission, the report ‘reaches’ the same cloud server hosting the data, becoming an integral part of the patient file for access, comparison, printing, sharing, data mining and data analysis in the future. Since November 2009, the ROP expert has been performing the same tasks of viewing and reporting on the iPhone (Apple Inc, Cupertino, USA). A validation of image quality on the iPhone vs on the Retcam Shuttle was performed before using it as the primary mode of reporting. Ten diagnoses were tested for agreement, namely (no ROP, stage 1, 2, or 3, aggressive posterior ROP, zone 1, 2, 3, pre plus and plus disease). Through the program iPhone 3GS, 4S and 5 have been used interchangeably by the reporting expert.
Tracking and follow-up
Every session is recorded in a special ROP register that is maintained in the NICU. the project manager keeps a hard copy. Each NICU has access to its own data (and none other) through this register. ‘ROP cards’ record the findings using the ICROP classification and the date and venue of the next follow-up is indicated, should the mother find another KIDROP center closer for follow-up. We make heavy use of mobile phones to contact the mothers via voice and text messages to remind them about the appointment in advance and if an appointment has been missed.
Laser photoablation is the primary modality of treatment and is performed using ETROP recommendations using 532nm green laser delivered by indirect ophthalmoscopy using standard guidelines. The top surface of the Retcam shuttle, without the laptop, is used to position the infant during treatment. Laser treatment is performed by KIDROP experts who visit the peripheral center, obviating the need for the infant to travel to the city. When not possible, travel costs to Bangalore are reimbursed.
Data were analyzed using SPSS (Version 17.0). Analysis included the agreement and correlation indices between the technician and ROP expert to diagnose and record follow up. This was compared between records of the ROP expert performing peripheral scleral depression with indirect ophthalmoscopy and comparing it with the technician's judgment recorded after each session using dynamic video assessment of his or her own recording. Both were masked to each other's records. Further, we analyzed agreement and correlation indices between the experts reporting on the iPhone vs on the primary Retcam laptop. The expert had access to the birth weight, gestational and post menstrual age at image capture, to allow a ‘real world’ experience during reporting. Other demographic details that could identify the patient or session were cropped or deleted. Ten percent of the images were repeated to allow inter-observer variability comparison.
Demographics and distribution
At the time of submission, 3 KIDROP ‘A teams’ servicing 81 enrolled NICU's in 18 districts in Karnataka have performed 41,237 imaging sessions (babies). Of these, 8503 sessions were performed during 2008-2009 and 22,596 performed during 2011-2102. Sessions for analysis of this manuscript were derived from these two timed cohorts. In 2010-2011, 227 sessions were included for the iPhone app validation analysis.
In 2008, the first 4,422 sessions were used for training two primary KIDROP technicians (Level 1). The subsequent 1462 sessions in 2008-09 and 455 sessions by the same technicians upgraded to Level III in 2011-12 were included for kappa correlation and agreement analysis between the technician and ROP expert. The distribution of these 6339 sessions (1601 infants) is summarized in Table 3 and shows that 36.4% of babies had 3 or less imaging sessions before discharge, the remaining (63.6%) had 4 or more sessions.
The distribution of the birth-weight plotted along the gestational age for screened and treated babies is depicted in [Fig. 1] and emphasizes that 28.5% of all infants treated had birth weights of > 1501gm and 6.3% of these ‘outliers’ had birth weights of > 2000gm.
Level I technicians agreed with 85.9% of all management (red, orange and green) of the expert. This improved to 94.3% of all decisions when they upgraded to Level III. The proportion of sessions where the technicians’ management decisions were non-referral when the expert thought this to be indicated dropped from 4.7 to 0.9% (Level I to III). This clinical utility score is summarized in Table 4. Of the 4 infants who were false negatives, two were called ‘red’ by the specialist and ‘orange’ (“follow up within a week”) by the technician and could have potentially been lost. The other 2 were marked ‘orange’ (zone 3 avascular) by the specialist and ‘green’ (mature retina) by the technician and arguably would not acquire ‘blinding’ disease even if missed. Hence, a Level III technician would miss only 0.4% (and not 0.9%) of infants with treatable lesions. Applying this correction to Level I, only 13 (and not 68 infants) [0.9% (13/1462)] would risk missing treatment.
The sensitivity, specificity, positive predictive value and negative predictive values for diagnosing ‘any stage of ROP’ and ‘treatment grade ROP’ during their transition from Level I to III are summarized in Table 5. The discriminatory index [(sensitivity x specificity)/100)] improved from 79.5 to 92.7 and 71.6 to 89.2 for ‘any stage’ and ‘treatment grade ROP’ respectively. The measurement of agreement (kappa) comparing 1) treatment vs no treatment 2) mild vs severe ROP and 3) discharge vs no discharge is summarized in Table 6, which again demonstrates significant improvement as their skills improved.
The overall agreement for all 10 categories of diagnoses was 96.3%. The measurement of overall agreement for detecting ROP was kappa 0.96 (SE 0.014, P< 0.0001), for type 1 ROP was kappa 0.96, (SE 0.024, P< 0.0001) and for mild, Type 2 ROP, was kappa 0.94, (SE 0.037, P< 0.0001). The sensitivity, specificity, positive and negative predictive values for severe and mild disease detections are summarized in Table 7.
India, like many other middle-income countries is facing the ‘third epidemic’ of ROP. Over the past two decades, ROP has been reported from major cities of the country with an incidence ranging between 37-54%. Infants blind from ROP continue to present to tertiary level facilities, many of whom have not been screened. Significantly, over the past decade, India has made steady progress in child health care indices and the infant mortality rate (IMR) has dropped from 81/1,000 live births in 1990 to 47/1,000 live births in 2011. This has led to an increase in surviving neonates, many of whom are preterm, even in rural centers which adds to the unmet challenge of ROP screening compounded by inadequate awareness among pediatricians, gynecologists and lack of sufficiently trained ROP specialists.
Telemedicine for ROP using pediatric wide-field digital retinal imaging with ‘remote experts’ who grade images is a successful means of bridging this gap. In most ‘real-world’ programs, images captured by nurses, ophthalmic photographers or ophthalmologists are read onsite or remotely by ‘ROP experts’ using a direct, ‘store and forward’ or image transfer platforms within a defined time period which could vary from a day to a week. However, in India, finding the ‘ROP expert’ albeit for remote reading is a huge challenge. With less than 500 registered vitreo-retinal surgeons, it is believed that there are less than 30-35 ROP experts who could provide comprehensive ROP care, and mostly reside in urban areas.
We began KIDROP with the belief that a telemedicine program will not solve our problem unless non-physicians can be trained not only to take images, but also to reliably grade them and make management decisions at the time of image capture. This is particularly important in India where larger, more mature infants develop severe ROP, many of whom have already been discharged from neonatal care. A delay in receiving the management decision from experts would pose an enormous administrative challenge in transmitting the management decision to parents, many of whom are poor, uneducated and who live at a distance from the neonatal center. To our best knowledge, in 2008 this was the first program to train technicians to capture and interpret retinal images. We evolved a training and accreditation score (STAT, Table 1) for this purpose. The aim was to provide the mother with a definitive diagnosis and date for the next visit even before she left the neonatal unit. Simultaneously, we tested remote reading by the ROP expert at our headquarters on an indigenously created tele-ROP platform that was enabled on the laptop and smart phone (iPhone) with ‘near-live’ reporting.
KIDROP was built on a “Triple-T” principle, namely T elemedicine, T raining of peripheral ophthalmologists and ophthalmic assistants and T aking the support of neonatologists, pediatricians and gynecologists. The program expanded from 6 pilot districts of Southern Karnataka to 18 districts in all, 12 of these supported by the National Rural Health Mission, Ministry of Health and Family Welfare, Government of Karnataka in the nation's first public private partnership in infant blindness prevention. At the time of submission, 81 neonatal units are serviced by 3 ‘A’ teams and 12 ‘B’ teams (local districts). Over 41,000 screening sessions have been performed using 4 Retcam shuttles and over 860 (10.2% of infants screened) infants have received treatment for ROP.
Previous ‘real-world telemedicine programs’ from Canada, United States, and Germany have used trained ophthalmologists or experts to remotely read and interpret images with different terminologies such as referral warranted ROP (RW-ROP) or clinically significant ROP (CS-ROP) for decision algorithms. We chose a new triage graded protocol based on the new ICROP classification which places emphasis on the management decision using a colour coding of red, orange and green [Table 2] keeping in mind the nature of demands on a non-physician grader in a remote area. This was conceived so as to create a wider safety net wherein, for example, Type 1 ROP is marked red, stage 1 is followed up (orange) and only mature retina, or definitely regressing ROP is discharged (green) [Fig. 2]. Another layer in the safety net is that no infant in our program is discharged until a mature retina is imaged on two consecutive visits, one of these between 41-45 weeks of postmenstrual age.
Our results demonstrate that Level I technicians have an overall agreement of 85.9% with the expert and this improves to 94.3% when they upgrade to Level III. In our setting, it takes an average of 30 and 90 working days to achieve a skill level of Level I and III respectively. In a screening program of this nature, missing treatable disease could be dangerous, as the child may never have access to a clinical exam by an ROP specialist. Our results show that this occurrence is indeed very low. A Level I technician would miss 0.9% of infants needing treatment and a Level III only 0.4%. The corollary would be the ‘false positives’, which could add the burden of another visit for the baby and the family. This nearly halves from 9.4% to 4.8% as the skill improves from Level I to III. This can be attributed to their ability to image the temporal periphery up to and including the ora serrata in an increasing proportion of babies, enhancing their confidence of ‘discharging’ the baby [Fig. 2]. Initially Level I technicians begin by uploading all cases (green, orange and red) for remote expert tele-reporting. With increased expertise, Level III technicians are able to triage better, with the more urgent ‘red’ cases being uploaded for the ROP specialist to confirm if treatment is required on the live tele-ROP platform. Despite high grades of agreement with the specialist, it is recommended that before a baby is discharged from the screening network, the ROP specialist ratifies this decision by viewing the images or examines the baby on site wherever possible.
In the United Kingdom, under the NHS Diabetic Eye Screening Programme, technicians from designated central reading centers are employed to interpret downloaded images for diabetic retinopathy changes. In the KIDROP program, our technicians capture, read and report ROP images ‘on-site’ and real-time. In future, with increasing volumes of images coming from different parts of the country, central-reading centers may become necessary.
We developed the smart phone app on the iPhone (Apple, CA, USA) for rapid review and reporting. In 2009, this was the first smart phone to provide touch technology, ‘pinch and drag’, and PDF printing compatibility. This app allowed the expert anytime access to the images, less dependence on the computer, a user friendly interface to report the diagnosis and suggest follow-up. This is tightly integrated with the database maintained on a cloud-based server and is compliant with regulatory standards. With the proliferation and improvement of smart phone technology, future research would include imaging using the smart phone, App based data management systems and integration with video conferencing.
A limitation of this study program is that it judged the validity of non-physicians to be graders with the assumption that the ‘gold standard’ for comparison of wide field digital imaging for ROP is dilated indirect ophthalmoscopy. This concept has already been questioned. Studies suggest that photographic documentation may ‘inadvertently’ detect mild disease that was ‘missed’ on ophthalmoscopic examination. The ability of images to document, review, store and compare disease far outweighs routine indirect ophthalmoscopy, even when performed by an expert. In our country, the current limited expertise to use ophthalmoscopy, particularly in rural areas is a case in favor of non-physician grading. The importance of training and validating the technicians cannot be overemphasized. Another limitation is that the cost-utility of this program has not been formally analyzed. Furthermore, the expertise of other Level III technicians has not been compared against our primary technicians who enjoy over 15,000 sessions each, hence making generalizability an unmeasured entity.
The KIDROP model is now being replicated in two more states and training is completed in two more. Level III technicians are the first line decision makers in the rural periphery who are backed by remote experts who read these images on smart phones. The outcome from these centers is awaited. However, the applicability of this program in other developed countries would attract unaddressed medico-legal constraints and needs evaluation.
In India, as ROP care, awareness, training and expertise among general ophthalmologists and specialists improves, it is likely that there would be less dependence on a program built on the tenants of KIDROP. Until then, the societal impact of missed screening due to lack of trained resources in peripheral areas leading to increased infant blindness would certainly be a factor for considering a ‘KIDROP like program’ as a model for ROP screening in underserved areas.
We acknowledge Mr. Praveen Sharma, Mr. Sivakumar Munusamy, Mr. Krishnan Narashimha for their participation in the program.
1. Gilbert C, Fielder A, Gordillo L, Quinn G, Semiglia R, Visintin P, et al International NO-ROP Group. Characteristics of infants with severe retinopathy of prematurity in countries with low, moderate, and high levels of development: Implications for screening programs Pediatrics. 2005;115:e518–25
2. Gilbert C. Retinopathy of Prematurity in middle-income countries Lancet. 1997;350:12–4
3. . Born to Soon. The Global Action Report on Preterm Birth United Nations. 2012Last accessed on 2013 Dec 31 Available from: http://www.who.int/pmnch/media/news/2012/201204_borntoosoon-report.pdf
4. . National Neonatology Forum of India. National Neonatal Perinatal Database Report for year 2003-2004. 2005 New Delhi
5. Vinekar A, Dogra MR, Sangtam T, Narang A, Gupta A. Retinopathy of prematurity in Asian Indian babies weighing greater than 1250 grams at birth: Ten years data from a tertiary care center in a developing country Indian J Ophthalmol. 2007;55:331–6
6. Sanghi G, Dogra MR, Katoch D, Gupta A. Demographic profile of infants with stage 5 retinopathy of prematurity in North India: Implications for screening Ophthalmic Epidemiol. 2011;18:72–4
7. Hungi B, Vinekar A, Datti N, Kariyappa P, Braganza S, Chinnaiah S, et al Retinopathy of prematurity in a rural neonatal intensive care unit in South India - A prospective study Indian J Pediatr. 2012;79:911–5
8. Vinekar A, Avadhani K, Braganza S, Shetty B, Dogra M, Gilbert C. Outcomes of a protocol-based management for zone 1 retinopathy of prematurity: The Indian Twin Cities ROP Screening Program report number 2 (Letter) Am J Ophthalmol. 2011;152:712
9. Vinekar A. IT-enabled innovation to prevent infant blindness in rural India: The KIDROP experience J Indian Bus Res. 2011;3:98–102
10. Vinekar A, Avadhani K, Dogra M, Sharma P, Gilbert C, Braganza S, et al A novel, low-cost method of enrolling infants at risk for Retinopathy of Prematurity in centers with no screening program: The REDROP study Ophthalmic Epidemiol. 2012;19:317–21
11. Jain R, Manikutty S. Narayana Nethralaya: A precious gift to a premature child Indian Institute of Management. 2011 Ahmedabad:1–18 IIMA/IITCOE0004
12. Vinekar A. The ROP challenge in rural India: preliminary report of a telemedicine screening model International Experience with Photographic Imaging for Pediatric and Adult Eye Disease, Retinal Physician.:9–10
13. . Vinekar. A Telemedicine Success Story for a population in dire need Retinal Physician. 2011:56–9
14. Vinekar A. Training is the Crux of a Telemedicine Program Ophthalmology World Report. 2010:8–10
15. McGrath D. ROP Screening Improves: Telemedicine Success Story in the Fight Against ROP Eurotimes. 2012:17
16. Pejaver RK, Vinekar A, Bilagi A National Neonatology Foundation's Evidence Based Clinical Practice Guidelines for Retinopathy of Prematurity, NNF India, Guidelines. 2010:253–62
17. Govindrajan V A telemedicine innovation for the poor that should open eye, Harvard Business Review. 2010Last accessed on 2013 Dec 31 Available from: http://blogs.hbr.org/govindarajan/2010/11/a-telemedicine-innovation-for-the-poor-that-should-open-eyes.html
18. . India Perspectives. Unique experiment in tele-medicine: Tele-ophthalmology provides a new hope in preventing infant blindness in rural India Perspectives. 2010;Vol. 24:70–1
19. . India Today Top ten medical innovations: iPhone used to stave off blindness, India Today. 2009;vol. 28:126–30
20. Kreatsoulas J Progress in ROP management through tele-ophthalmology, Retina Today. 2010
21. Rai A Telemedicine in India moves onto version 2.0, Economic Times. 2010:6–7
22. Balasubramanian M, Capone A Jr, Hartnett ME, Pignatto S, Trese MT. Photographic Screening for Retinopathy of Prematurity (Photo-ROP) Cooperative Group. The Photographic Screening for Retinopathy of Prematurity Study (Photo-ROP): Study design and baseline characteristics of enrolled patients Retina. 2006;26(Suppl 7):S4–10
23. Vinekar A, Trese MT, Capone A Jr. Photographic Screening for Retinopathy of Prematurity (PHOTOROP) Cooperative Group. Evolution of retinal detachment in posterior retinopathy of prematurity: Impact on treatment approach Am J Ophthalmol. 2008;145:548–55
24. Golnik C, Beaver H, Gauba V, Lee AG, Mayorga E, Palis G, et al Development of a new valid, reliable, and internationally applicable assessment tool of residents’ competence in ophthalmic surgery (An American Ophthalmological Society Thesis) Trans Am Ophthalmol Soc. 2013;111:24–33
25. . International Committee for the Classification of Retinopathy of Prematurity. The International Classification of Retinopathy of Prematurity revisited Arch Ophthalmol. 2005;123:991–9
26. . Early treatment of Retinopathy of Prematurity cooperative group. Revised indications for the treatment of retinopathy of prematurity: Results of the early treatment of Retinopathy of Prematurity Randomized trial Arch Ophthalmol. 2003;121:1684–96
27. Dogra MR, Vinekar A, Viswanathan K, Sangtam T, Das P, Gupta A, et al Laser treatment for retinopathy of prematurity through the incubator wall Ophthalmic Surg Lasers Imaging. 2008;39:350–2
28. Charan R, Dogra MR, Gupta A, Narang A. The incidence of retinopathy of prematurity in a neonatal care unit Indian J Ophthalmol. 1995;43:123–6
29. Gopal L, Sharma T, Ramchandran S, Shanmugasundaram R, Asha V. Retinopathy of prematurity. A study Indian J Ophthalmol. 1995;43:50–61
30. Jalali S, Anand R, Kumar H, Dorgra MR, Azad EV, Gopal L. Programme planning and screening strategy in retinopathy of prematurity Indian J Ophthalmol. 2003;51:89–97
32. Richter GM, Williams SL, Starren J, Flynn JT, Chiang MF. Telemedicine for Retinopathy of Prematurity Diagnosis: Evaluation and Challenges Surv Ophthalmol. 2009;54:671–85
33. Chiang MF, Wang L, Busuioc M, Du YE, Chan P, Kane SA, et al Telemedical retinopathy of prematurity diagnosis: Accuracy, reliability, and image quality Arch Ophthalmol. 2007;125:1531–8
34. Murakami Y, Jain A, Silva RA, Lad EM, Gandhi J, Moshfeghi DM. Stanford University Network for Diagnosis of Retinopathy of Prematurity (SUNDROP): 12-month experience with telemedicine screening Br J Ophthalmol. 2008;92:1456–60
35. Scott KE, Kim DY, Wang L, Kane SA, Coki O, Starren J, et al Telemedical diagnosis of retinopathy of prematurity intraphysician agreement between ophthalmoscopic examination and image-based interpretation Ophthalmology. 2008;115:1222–8
36. Skalet AH, Quinn GE, Ying GS, Gordillo L, Dodobara L, Cocker K, et al Telemedicine screening for retinopathy of prematurity in developing countries using digital retinal images: A feasibility project J AAPOS. 2008;12:252–8
37. Yen KG, Hess D, Burke B, Johnson RA, Feuer WJ, Flynn JT. Telephotoscreening to detect retinopathy of prematurity: Preliminary study of the optimum time to employ digital fundus camera imaging to detect ROP J AAPOS. 2002;6:64–70
38. Chiang MF, Keenan JD, Starren J, Du YE, Schiff WM, Barile GR, et al Accuracy and reliability of remote retinopathy of prematurity diagnosis Arch Ophthalmol. 2006;124:322–7
39. Chiang MF, Starren J, Du YE, Keenan JD, Schiff WM, Barile GR, Li J, et al Remote image based retinopathy of prematurity diagnosis: A receiver operating characteristic analysis of accuracy Br J Ophthalmol. 2006;90:1292–6
40. Roth DB, Morales D, Feuer WJ, Hess D, Johnson RA, Flynn JT. Screening for retinopathy of prematurity employing the retcam 120: Sensitivity and specificity Arch Ophthalmol. 2001;119:268–72
41. Wu C, Petersen RA, VanderVeen DK. Retcam imaging for retinopathy of prematurity screening J AAPOS. 2006;10:107–11
42. Ells AL, Holmes JM, Astle WF, Williams G, Leske DA, Fielden M, et al Telemedicine approach to screening for severe retinopathy of prematurity: A pilot study Ophthalmology. 2003;110:2113–7
43. Lorenz B, Spasovska K, Elfein H, Schneider N. Wide-field digital imaging
based telemedicine for screening for acute retinopathy of prematurity (ROP).Six-year results of a multicentre field study Graefes Arch Clin Exp Ophthalmol. 2009;247:1251–62
44. Schwartz SD, Harrison SA, Ferrone PJ, Trese MT. Telemedical evaluation and management of retinopathy of prematurity using a fiberoptic digital fundus camera Ophthalmology. 2000;107:25–8
45. Shah PK, Narendran V, Saravanan VR, Raghuram A, Chattopadhyay A, Kashyap M. Screening for retinopathy of prematurity--A comparison between binocular indirect ophthalmoscopy and RetCam 120 Indian J Ophthalmol. 2006;54:35–8
46. Moshfeghi DM, Capone A JrHartnett ME, Trese M, Capone A. Telemedicine Pediatric Retina. 2013 Philadelphia Wolters Kluwer:523–32
47. . Diabetic Retinopathy Guidelines The Royal College of Ophthalmology, United Kingdom. 2012:1–147
48. Trese MT. What is the real gold standard for ROP screening? Retina. 2008;28(Suppl 3):S1–2
Source of Support: Nil.
Conflict of Interest: None declared.