REVIEW URRENT C OPINION
Diabetic retinopathy screening and the use of telemedicine Ingrid E. Zimmer-Galler a, Alan E. Kimura b, and Sunil Gupta c
Purpose of review Evidence-based practice guidelines and treatments are highly effective in reducing vision loss from diabetic retinopathy. However, less than half of the total number of patients with diabetes mellitus receive recommended annual retinal evaluations, and vision loss due to diabetic retinopathy remains the leading cause of blindness in adults. Poor adherence to screening recommendations stems from a number of challenges which telemedicine technology may address to increase the evaluation rates and ultimately reduce vision loss. The aim of this review was to provide an update on the recent advances in teleophthalmology and how it may expand our current concept of eye care delivery for diabetic eye disease. Recent findings The benefits of telemedicine diabetic retinopathy are proven for large population-based systems. Outcomes information from community-based programs is now also beginning to emerge. Improved screening rates and less vision loss from diabetic retinopathy are being reported after implementation of telemedicine programs. New imaging platforms for telemedicine programs may enhance the ability to detect and grade diabetic retinopathy. However, financial factors remain a barrier to widespread implementation. Summary Telemedicine diabetic retinopathy screening programs may have a significant impact on reducing the vision complications and healthcare burden from the growing diabetes epidemic. Video abstract http://links.lww.com/COOP/A17 Keywords diabetic retinopathy screening, healthcare delivery, telemedicine, tele-ophthalmology, teleretinal screening
INTRODUCTION The ‘Triple Aim’ is a health policy strategy often used as a touchstone for 21st century healthcare reform in the USA [1]. Telemedicine aligns well with the ‘Triple Aim’ objectives to improve the health of populations, improve the patient experience of their care, and reduce per capita cost of healthcare. The global prevalence of diabetes mellitus is estimated to increase to 439 million affected adults worldwide by 2030 [2]. The diabetes epidemic will necessitate progressive approaches to care of the disease and its complications. Early detection, accurate diagnosis, and timely treatment of visionthreatening diabetic retinopathy have long been established as a means to significantly reduce vision loss from diabetes and improve population health. Multiple professional organizations, including the American Academy of Ophthalmology, recognize the minimum requirement of an annual retinal evaluation for patients with diabetes. Despite these
recommendations, a substantial proportion of patients with diabetes worldwide still do not receive recommended eye care. In the USA, only approximately half of the diagnosed population with diabetes is screened annually for diabetic retinopathy, perpetuating little change over several decades [3]. Vision loss and greater healthcare and societal costs result when patients with diabetes present for eye
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Wilmer Eye Institute, Johns Hopkins University Medical Institutions, Baltimore, Maryland, bDepartment of Ophthalmology, University of Colorado Health Sciences Center, Anschutz Medical Campus, Aurora, Colorado, USA and cRetina Specialty Institute, Pensacola, FL, USA Correspondence to Ingrid E. Zimmer-Galler, MD, Wilmer Eye Institute, Johns Hopkins University Medical Institutions, 600 N Wolfe Street, Maumenee 738, Baltimore, MD 21287, USA. Tel: +1 301 620 9268; e-mail: [email protected] Curr Opin Ophthalmol 2015, 26:167–172 DOI:10.1097/ICU.0000000000000142
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KEY POINTS Telemedicine applications may be utilized to increase diabetic retinopathy assessment rates and may decrease vision loss from diabetic eye disease. New imaging technologies, such as wide-field imaging and optical coherence tomography, may provide additional benefits for telemedicine identification of diabetic retinopathy, but the cost may preclude widespread use. Financial factors remain a major challenge for long-term viability and widespread implementation of telemedicine diabetic retinopathy programs in the USA.
outlining essential components including a robust technology platform, quality assurance procedures, efficient workflows, cost–effectiveness and adequate reimbursement, as well as compliance with legal and regulatory requirements [6]. Rigorous validation to ensure the program meets evidence-based standards of care is essential [6,7]. Over the past decade, many telemedicine diabetic retinopathy programs have published their validation studies demonstrating various successful aspects of the technology, including quality of remotely acquired retinal images, accuracy of remote diagnosis, and early increases in rates of screening for diabetic retinopathy. The overall diagnostic accuracy of telemedicine diabetic retinopathy screening is high, with sensitivity exceeding 80% and specificity of 90% or greater in most published studies [8 ]. Only recently, however, are actual outcomes data becoming available from wide-scale deployments of this technology. This review will explore the current state of telemedicine for diabetic retinopathy assessment, with an emphasis on recent developments and future directions. &
care late in the disease course with delayed diagnosis of a treatable condition. Telemedicine is a striking example of the disruptive innovation required to improve upon key aspects of the healthcare system [4]. Acquisition of retinal images at the point of care in primary care locations outside of the traditional eye care arena can improve patients’ care experience. Remote imaging to detect possible vision-threatening pathology in patients with diabetes, who may be asymptomatic, bridges many barriers such as transportation, concern with pupillary dilation and poor adherence to recommendations for eye evaluations. Reducing the cost of care remains an enduring policy objective in healthcare. The Affordable Care Act of 2010 expands insurance and begins to experiment with new healthcare delivery and financing models [5]. Medicare, Medicaid, and private insurers must create a sustainable financial model for innovations like tele-ophthalmology. Cost avoidance should also be considered in the economic analysis since early detection and treatment resulting from telemedicine diabetic retinopathy screening may generate significant savings in the long term by minimizing progression to late-presenting advanced disease. The use of telemedicine with remote retinal imaging has been shown to be possible across a broad range of populations and geographic areas. Various approaches to teleretinal screening include mydriatic versus nonmydriatic imaging, single field or multiple field imaging, stereoscopic versus monoscopic imaging, and variable threshold levels of diabetic retinopathy dictating when referral is necessary. A tailored approach to the development and implementation of an effective telemedicine diabetic retinopathy assessment program is necessary and is dictated by the program’s goals and objectives. The American Telemedicine Association has published guidelines 168
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CURRENT STATUS OF TELEMEDICINE FOR DIABETIC RETINOPATHY In 2005, the Department of Veterans Affairs instituted what is now the largest telemedicine diabetic retinopathy assessment program implemented in the USA. It is estimated that 90% of the Veterans with diabetes currently undergo an annual evaluation for diabetic retinopathy [9 ]. Kirkizlar et al. [10 ] performed a retrospective random review of 900 Veterans Affairs medical records from a cohort of approximately 9000. Trends by year, for 5 years after implementation of the diabetic retinopathy screening program, were evaluated and showed increasing screening rates, decreasing age of patients undergoing screening, increasing percentage of non-Caucasians receiving screening, and decreased average number of miles traveled for screening. This provides further evidence that large-scale telemedicine programs have a role in increasing adherence to recommended evaluations and in increasing access for different patient populations. Additional information from the Veterans Affairs teleretinal screening program describes the effect of community-based diabetic retinopathy assessment on eye care use and medical center resources. Data from almost 2000 diabetic retinopathy screening events at one Veterans Affairs center over a 6-month period were used to calculate use ratios which may be useful to predict the added resources needed to care for newly referred patients from diabetic retinopathy screening programs [9 ]. &
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The results from the Veterans Affairs teleretinal program alleviate concerns that remote retinal imaging programs may divert patients away from traditional eye care settings. While the task of evaluating all patients with diabetes for the presence of diabetic retinopathy is enormous, there is no evidence to date that telemedicine diabetic retinopathy programs will result in unmanageable referral rates. The Scottish National Diabetic Retinopathy Screening Program has reviewed referral rates over the first 5 years after program introduction in 2006 [11 ]. Out of a total of 225 442 patients eligible for screening for diabetic retinopathy, 187 822 (83.3%) were imaged at least once. There were 560 362 screening episodes during the 5-year study period. Referral rates were greatest in the first 2 years of the program and then remained steady for the following 3 years. This suggests that within 2 years of implementation, the program successfully screened most persons who were previously not evaluated. Referable disease was more commonly found at an individual’s initial screening evaluation and, after the initial increase in referrals, rates stabilized. The most successful telemedicine diabetic retinopathy assessment program in terms of sheer volume is the UK National Health Service Diabetic Eye Screening Program, which now annually assesses almost 2 million patients with diabetes. In an exciting development, Liew et al. [12 ] compared blindness certifications in England and Wales between 1999–2000 and 2009–2010. The leading cause of blindness, out of 1637 certifications received between 1999 and 2000, was diabetic retinopathy. A decade later, the leading cause of blindness, out of 1756 certifications, was hereditary retinal disorders. They concluded, ‘For the first time in at least five decades, diabetic retinopathy/maculopathy is no longer the leading cause of certifiable blindness among working age adults in England and Wales’. They postulate that this change is at least in part related to introduction of nationwide diabetic retinopathy screening programs. A major limitation of this study is that blindness certifications in the United Kingdom are not compulsory and perhaps not all eligible patients were registered as blind. Nonetheless, this is a powerful information indicating for the first time that longterm and wide-scale diabetic retinopathy screening may have an impact on actually reducing vision loss in a large population. &
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ADVANCES IN OCULAR TELEMEDICINE TECHNOLOGY Early Treatment Diabetic Retinopathy Study (ETDRS) 7-field stereo photography (currently performed with digital imaging rather than film) remains the gold standard for detection of diabetic retinopathy and
clinically significant macular edema, and is also the standard against which most diabetic retinopathy screening programs are validated [13]. ETDRS fundus photography is not suitable as a screening tool because it requires an expert photographer and pupil dilation, is time-consuming, and is not efficient for screening purposes. Most screening diabetic retinopathy programs therefore have modified imaging protocols including only one or a few posterior retinal fields. New information suggests that these protocols may be missing significant diabetic pathology. The development of nonmydriatic wide-field cameras may offer an opportunity to optimize photography for diabetic retinopathy screening. With the use of scanning laser ophthalmoscopy (SLO), nonmydriatic imaging covering 180–200 degrees of the retina is possible and has demonstrated significant utility for enhanced diagnosis, treatment, and monitoring of retinal disease. Several investigators have reported on substantial agreement between wide-field SLO and mydriatic 7-field fundus photography for grading diabetic retinopathy [14,15,16 ,17 ]. Silva et al. [18 ] found that one-third of hemorrhages, microaneurysms, intraretinal microvascular abnormalities, and neovascularization were localized outside the coverage area of the ETDRS fields, which resulted in a more severe diabetic retinopathy grade in 10% of the cases. Furthermore, nonmydriatic SLO imaging is technically easy to perform by office staff without expertise. It has also been shown to significantly reduce the unreadable image rate to less than 3% and reduce image evaluation time by 28% when compared with standard fundus photography [19 ]. At present, the main deterrent to large-scale deployment of SLO technology in primary care settings is the substantial cost of the devices, which currently exceeds US $60 000. Investigators from the UK screening program evaluated incorporation of optical coherence tomography (OCT) in addition to retinal photography for patients with surrogate markers for macular edema such as hard exudates [20]. Within the UK program, selective addition of OCT to the screening pathway was cost effective by improving detection of macular edema. The addition of OCT technology to diabetic retinopathy screening programs needs further investigation, but in other healthcare systems, such as in the USA, the additional equipment costs may be prohibitive for screening purposes. &&
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CHALLENGES FOR TELEMEDICINE DIABETIC RETINOPATHY PROGRAMS: FINANCIAL FACTORS In the USA, the Veterans Affairs (and Indian Health Service) telemedicine diabetic retinopathy programs
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are funded by recurring federal appropriations. Many additional diabetic retinopathy screening programs were initially established with grant support, but ultimately proved to not be financially viable for ongoing clinical operation after funding was exhausted. Few large private telemedicine diabetic retinopathy programs have been successful in the long term in the USA because financial sustainability remains a major challenge without additional funding sources. Several different business models for telemedicine diabetic retinopathy programs exist. The most common arrangement utilizes the primary care arena as the point of service where retinal images are acquired. The images and patient demographics are transmitted to a remote reading center for expert assessment and a report is returned to the primary care provider detailing whether referral to an ophthalmologist is necessary. The retinal camera may be purchased or leased by the primary care physician who has an agreement with a reading center for image interpretation. Reimbursement is usually divided into image capture (technical) and image interpretation (professional) components for the primary care office and reading center, respectively. Computing and telecommunications costs are no longer a barrier, and broad bandwidth is almost universally available and inexpensive. However, retinal cameras continue to approach US $15 000 to US $20 000 including installation and servicing which is often too costly for individual primary care offices with limited numbers of patients with diabetes. Research and development has been ongoing for over a decade, but a true low-cost (less than US $1000) validated nonmydriatic retinal camera is still not available. An interesting area of study is the use of smartphone technology as an inexpensive fundus camera. Many technical issues remain and currently there are no validated smartphone camera systems in use with image quality adequate for teleretinal screening, but the possibility of an inexpensive, widely available, portable, and wireless imaging platform is intriguing [21 ,22 ]. Studies on the cost–effectiveness of the Veterans Affairs and UK telemedicine diabetic retinopathy programs have been performed, but these results are not directly applicable to programs being implemented in community primary care settings in the USA [9 ,20]. Limited current information on the cost effectiveness of diabetic retinopathy screening in community settings in the USA is available in the literature. The costs of screening can vary considerably. In one community-based program for disadvantaged patients, the cost of screening per patient was estimated to be US $100 [23]. In the first 18 months after implementation, Harris Health &
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System in Houston, Texas, in collaboration with a commercially available telemedicine diabetic retinopathy assessment program (Intelligent Retinal Imaging Systems, Pensacola, Florida, USA), was able to achieve an increase in diabetic retinopathy screening rates from 62 to 86% in a population of 48 000 patients with diabetes. The screening cost per patient was calculated to be less than US $50 for the 27 302 unique patients screened [24]. Not only is reimbursement for telemedicine diabetic retinopathy services not adequate to cover these costs, it presents a very confusing landscape at present. Traditionally, Current Procedural Terminology (CPT) code 92 250 for fundus photography was used to bill for diabetic retinopathy telemedicine services. In 2011, new remote retinal imaging CPT codes 92 227 and 92 228 were introduced. However, these codes are difficult to use as they do not adequately describe the work being performed by most telemedicine programs and they do not adequately cover the costs associated with teleretinal screening. The descriptor for CPT code 92 227 is remote imaging for detection of retinal disease under physician supervision, which implies that a nonlicensed provider interprets the images. The reimbursement is very low (less than US $15) because there is no compensation for physician work. The descriptor for CPT code 92 228 is remote imaging for monitoring and management of active retinal disease with physician review, interpretation and report. While reimbursement is somewhat higher (less than US $40), CPT code 92 228 can only be used for patients in whom diabetic retinopathy, or active disease, is present, which is generally a minority of the patients being screened. Furthermore, there are inconsistent coverage policies among Medicare carriers, and often neither of the two remote retinal imaging codes is covered. The lack of adequate reimbursement for telemedicine diabetic retinopathy assessment continues to be a major barrier to widespread implementation. Some of the current prohibitive financial barriers for implementation of diabetic retinopathy telemedicine programs may be mitigated in the future as pay-for-performance and penalties for missing key quality measures become more substantial. However, incorporating new and more expensive imaging technology into diabetic retinopathy assessment programs will further complicate the financial sustainability of these programs.
QUALITY ASSURANCE AND CONTROL In order to achieve the highest possible standards, quality metrics are an integral component of a telemedicine diabetic retinopathy assessment program. Volume 26 Number 3 May 2015
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Quality assurance focuses on continuously assessing performance, whereas quality improvement focuses on enhancing performance. Ocular telehealth programs should have protocols in place to monitor and evaluate performance of all components of the program, including assessment rates, gradeability of images, quality of grading, timeliness of reports, and follow-up of screen-positive patients. Continued education and certification of persons acquiring images, as well as graders, should be emphasized in addition to adherence to established protocols. Whereas the United Kingdom has quality standards and key performance indicators in place, further investigation is needed to establish uniform quality metrics for diabetic retinopathy screening programs in the USA [25].
FUTURE DIRECTIONS To address the impact on healthcare resources from the expected global increase in the diabetes population, automation of retinal image evaluation by using computers to either assist or fully automate diabetic retinopathy evaluation will be a critical step in helping to decrease the burden of manual retinopathy evaluation while still providing quality eye care. Ultimately, automated retinal image analysis will be necessary to increase the efficiency of image grading in a cost-effective manner. The field is evolving rapidly, but at present there are no automated retinal image analysis algorithms with United States Food and Drug Administration (FDA) clearance for use in the USA. To date, most research efforts have focused on algorithm development rather than measuring the clinical impact and public health significance of the automated systems. A detailed discussion of the current work with these systems is beyond the scope of this review [26,27,28 ]. In addition to the potential for a smartphonebased fundus camera, a mobile phone-based tele-ophthalmology platform holds significant future promise. New applications and interfaces may augment healthcare delivery by allowing image interpretation, data collection, wireless transfer, and integration into electronic medical records [29]. Utilization of teleretinal technology to detect ocular disease other than diabetic retinopathy is in the early stages, and limited information exists in the literature assessing strategies for grading and detecting additional eye diseases in adults. However, diabetic retinopathy screening programs ultimately need to be powerful enough to identify other abnormalities, suggestive of disease that may lead to vision loss. Additionally, retinal images of some patients obtained through diabetic retinopathy assessment programs will invariably include abnormal findings
other than diabetic retinopathy. Glaucoma and agerelated macular degeneration, in particular, remain important causes of vision loss in the elderly, and the role for telemedicine technology in these diseases is being investigated [30 ,31,32 ]. &
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CONCLUSION The use of an ocular telemedicine approach for diabetic retinopathy assessment has the potential to expand our standard concept of eye care delivery by extending access to care, offering alternative methods for receiving appropriate care and integrating diabetes eye care into the patient’s total healthcare. As Dartmouth professor Batalden states, ‘If we keep doing what we have been doing, we’ll keep getting what we’ve always gotten’ – an expensive and inefficient healthcare system that screens only half of the known population with diabetes [33]. Acknowledgements None. Financial support and sponsorship None. Conflicts of interest S.G. is a consultant for Allergan, Alcon, and Genentech, owns stock/stock options for Intelligent Retinal Imaging Systems and has principal in USRetina.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest
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1. Berwick DM, Nolan TW, Whittington J. The triple aim: care, health and cost. Health Aff (Millwood) 2008; 27:759–769. 2. Shaw J, Sicree R, Zimmet P. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010; 87:4–14. 3. National Committee for Quality Assurance. The state of healthcare quality report 2014. ePub http://ncqa.org. [Accessed 2 December 2014] 4. Christenson CM, Grossman JH, Hwang J. The innovator’s prescription: a disruptive solution for healthcare. McGraw-Hill; 2008; pp. 123–125. 5. The Henry J. Kaiser Family Foundation. Summary of the affordable care act. http://kaiserfamilyfoundation.files.wordpress.com/2011/04/8061-021.pdf. [Accessed 15 December 2014] 6. Li H, Horton M, Bursell S, et al. Telehealth practice recommendations for diabetic retinopathy, second edition. Telemed EHealth 2011; 17:814–837. 7. Williams G, Scott I, Haller J, et al. Single-field fundus photography for diabetic retinopathy screening: a report by the American Academy of Ophthalmology. Ophthalmology 2004; 111:1055–1062. 8. Shi L, Wu H, Dong J, Jiang K, Lu X, Shi J. Telemedicine for detecting diabetic & retinopathy: a systematic review and meta-analysis. Br J Ophthalmol 2015; 1–9. [Epub ahead of print] This meta-analysis includes 20 publications and determined that diagnostic accuracy of telemedicine diabetic retinopathy detection is high. Diagnostic accuracy was higher for images obtained with mydriasis and with wide-field imaging. 9. Chasan J, DeLaune B, Maa A, Lynch M. Effect of a tele retinal screening & program on eye care use and resources. J Am Med Assoc Ophthalmol 2014; 132:1045–1051. This study evaluates measurable resource burdens to be anticipated from increased volume of clinical care as a result of implementation of a telemedicine diabetic retinopathy screening program.
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Retinal, vitreous and macular disorders 10. Kirkizlar E, Serban N, Sisson J, et al. Evaluation of telemedicine for screening of diabetic retinopathy in the Veterans Health Administration. Ophthalmology 2013; 120:2604–2610. Within the Veterans Administration health system, telemedicine diabetic retinopathy screening was found to be cost effective for patient populations greater than 3500 patients, patients less than 80 years of age, and all racial groups. After implementation of the telemedicine program, the average age of patients being screened decreased and the percentage of non-white patients receiving screenings increased. 11. Looker HC, Nyangoma SO, Cromie DT, Olson JA, Leese GP, Black MW, Doig & J, et al. Scottish Diabetes Research Network Epidemiology Group; Scottish Diabetic Retinopathy Collaborative. Rates of referable eye disease in the Scottish National Diabetic Retinopathy Screening Programme. Br J Ophthalmol 2014; 98:790–795. Referral rates for diabetic retinopathy and maculopathy were evaluated over a 5-year period after implementation of a national diabetic retinopathy screening program in Scotland. The yield of referable disease was greatest in the first two years and then stabilized for subsequent years. Suspected diabetic macular edema was the most common reason for referral. 12. Liew G, Michaelides M, Bunce C. A comparison of the causes of blindness && certifications in England and Wales in working age adults (16–64 years), 1999–2000 with 2009–2010. Br Med J Open 2014; 4:e004015. The leading cause of blindness certifications in England and Wales in 1999–2000 was diabetic retinopathy and maculopathy, whereas in 2009–2010, the leading cause of blindness certifications was hereditary retinal disorders. The fact that diabetic retinopathy is no longer the leading cause of certifiable blindness in England and Wales may be related to introduction of a nationwide diabetic retinopathy screening program as well as improved glycemic control. 13. Early Treatment Diabetic Retinopathy Research Study Group. Grading diabetic retinopathy from stereoscopic color fundus photographs: an extension of the modified Airlie House classification. ETDRS report number 10. Ophthalmology 1991; 98:786–806. 14. Kernt M, Hadi I, Pinter F, et al. Assessment of diabetic retinopathy using nonmydriatic ultra-widefield scanning laser ophthalmoscopy (Optomap) compared with ETDRS 7-field stereo photography. Diabetes Care 2012; 35:2459–2463. 15. Silva P, Cavallerano J, Sun J, et al. Nonmydriatic ultrawide field retinal imaging compared with dilated standard 7-field 35 mm photography and retinal specialist examination for evaluation of diabetic retinopathy. Am J Ophthalmol 2012; 154:549–559. 16. Rasmussen M, Broe R, Frydkjaer-Olsen U, et al. Comparison between Early && Treatment Diabetic Retinopathy Study 7: field retinal photos and nonmydriatic, mydriatic and mydriatic steered wide field scanning laser ophthalmoscopy for assessment of diabetic retinopathy. J Diabetes Complications 2015; 29:99–104. Nonmydriatic wide-field retinal images were compared with and matched favorably with mydriatic seven-field ETDRS photographs for 190 eyes in patients with diabetes mellitus. Overlapping eyelashes and distortion may result in missing some lesions with wide-field images. 17. Liegl R, Liegl K, Ceklic L, et al. Nonmydriatic ultra-wide-field scanning laser & ophthalmoscopy (Optomap) versus two-field fundus photography in diabetic retinopathy. Ophthalmologica 2014; 231:31–36. Nonmydriatic wide-field imaging of 143 eyes was compared with mydriatic twofield fundus photography for diabetic retinopathy grading. Overall correlation for grading diabetic retinopathy level was moderate and correlation was substantial for clinically significant macular edema. 18. Silva P, Cavallerano J, Sun J, et al. Peripheral lesions identified by mydriatic & ultrawide field imaging: distribution and potential impact on diabetic retinopathy severity. Ophthalmology 2013; 120:2587–2595. Mydriatic ultrawide-field imaging was compared with ETDRS seven field photography in 206 eyes. Substantial agreement was noted in determining diabetic retinopathy severity. Additional peripheral lesions were noted with ultrawide-field imaging resulting in more severe assessment of diabetic retinopathy than determined with ETDRS photographs in 10% of patients. &
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19. Silva P, Cavallerano J, Tolls D, et al. Potential efficiency benefits of nonmydriatic ultrawide field retinal imaging in an ocular telehealth diabetic retinopathy program. Diabetes Care 2014; 37:50–55. The efficiency of nonmydriatic fundus photography and nonmydriatic ultrawidefield imaging was compared in an ocular telehealth program. A more severe diabetic retinopathy severity level was suggested in 9% of eyes imaged with the wide-field technique. Additionally, the ungradable rate was reduced by 71% and the image evaluation time was reduced by 28% with ultrawide-field images suggesting improved efficiency of diabetic retinopathy teleretinal screening with wide-field imaging devices. 20. Prescott G, Sharp P, Goatman K, et al. Improving the cost-effectiveness of photographic screening for diabetic macular edema: a prospective, multicentre, UK study. Br J Ophthalmol 2014; 98:1042–1049. 21. Maamari R, Keenan J, Fletcher D, Margolis T. A mobile phone-based retinal & camera for portable wide field imaging. Br J Ophthalmol 2014; 98:438–441. The authors have developed a smart-phone based retinal camera with off-the-shelf components capable of wide-field imaging. A validation study for diabetic retinopathy assessment has not been performed with the camera. 22. Darma S, Zantvoord F, Verbraak FD. The quality and usability of smartphone & and hand-held fundus photography, compared to standard fundus photography. Acta Ophthalmol 2014; doi: 10.1111/aos.12632 [Epub ahead of print] Images from 27 eyes were obtained with a smartphone-assisted device, hand-held fundus photography device and standard fundus camera. Image quality of the smartphone set-up was far less than with standard fundus photography and less than with the hand-held device. 23. Byrne M, Parker D, Tannenbaum S, et al. Cost of a community-based diabetic retinopathy screening program. Diabetes Care 2014; 37:e236–e237. 24. Zimmer-Galler I, Silva P. Proceedings of 32nd Annual Meeting of American Society of Retina Specialists. 9–12 August 2014; San Diego, California. 25. NHS Diabetic Eye Screening Programme. http://diabeticeyescreening.nhs.uk. [Accessed 2 January 2015] 26. Trucco E, Ruggeri A, Karnowski T, et al. Validating retinal fundus image analysis algorithms: issues and a proposal. Invest Ophthalmol Vis Sci 2013; 54:3546–3559. 27. Abramoff M, Folk J, Han D, et al. Automated analysis of retinal images for detection of referable diabetic retinopathy. J Am Med Assoc Ophthalmol 2013; 131:351–357. 28. Abramoff MD, Niemeijer M. Mass screening of diabetic retinopathy using & automated methods. In Teleophthalmology in Preventive Medicine. Michelson G, editor. Berlin Heidelberg: Springer Verlag; 2015. Review of scientific studies of automated methods for mass screening evaluated on at least 300 persons with diabetes reveals they achieve a sensitivity of at least 80%. This suggests that automated methods for mass screening of diabetic eye disease have matured and are now safe to consider deployment in clinical practice. 29. Kumar S, Wang E, Pokabla M, Noecker R. Teleophthalmology assessment of diabetic retinopathy fundus images: smartphone versus standard office computer workstation. Telemed J EHealth 2012; 18:158–162. 30. Verma S, Arora S, Kassam F, et al. Northern Alberta remote tele glaucoma & program: clinical outcomes and patient disposition. Can J Ophthalmol 2014; 49:135–140. This study describes a successful tele-glaucoma program, which stratifies patients based on known risk factors and utilizes equipment in addition to a fundus camera. 31. Kassam F, Amin S, Sogbesan E, Damji K. The use of tele glaucoma at the University of Alberta. J Telemed Telecare 2012; 18:367–373. 32. Li B, Powell A, Hooper P, Sheidow TG. J Am Med Assoc Ophthalmol 2014. & [Epub ahead of print] This study, comparing telemedicine screening and monitoring for neovascular agerelated macular degeneration with retina specialist evaluation, found that telemonitoring results in longer time interval before treatment reinitiation, but does not lead to adverse visual outcomes and may decrease the burden of follow-up visits with retinal specialists. 33. McInnis D. What system? Dartmouth Med 2006;28–35. dartmed.dartmouth.edu.
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Diabetic retinopathy screening and the use of telemedicine Ingrid E. Zimmer-Galler a, Alan E. Kimura b, and Sunil Gupta c
Purpose of review Evidence-based practice guidelines and treatments are highly effective in reducing vision loss from diabetic retinopathy. However, less than half of the total number of patients with diabetes mellitus receive recommended annual retinal evaluations, and vision loss due to diabetic retinopathy remains the leading cause of blindness in adults. Poor adherence to screening recommendations stems from a number of challenges which telemedicine technology may address to increase the evaluation rates and ultimately reduce vision loss. The aim of this review was to provide an update on the recent advances in teleophthalmology and how it may expand our current concept of eye care delivery for diabetic eye disease. Recent findings The benefits of telemedicine diabetic retinopathy are proven for large population-based systems. Outcomes information from community-based programs is now also beginning to emerge. Improved screening rates and less vision loss from diabetic retinopathy are being reported after implementation of telemedicine programs. New imaging platforms for telemedicine programs may enhance the ability to detect and grade diabetic retinopathy. However, financial factors remain a barrier to widespread implementation. Summary Telemedicine diabetic retinopathy screening programs may have a significant impact on reducing the vision complications and healthcare burden from the growing diabetes epidemic. Video abstract http://links.lww.com/COOP/A17 Keywords diabetic retinopathy screening, healthcare delivery, telemedicine, tele-ophthalmology, teleretinal screening
INTRODUCTION The ‘Triple Aim’ is a health policy strategy often used as a touchstone for 21st century healthcare reform in the USA [1]. Telemedicine aligns well with the ‘Triple Aim’ objectives to improve the health of populations, improve the patient experience of their care, and reduce per capita cost of healthcare. The global prevalence of diabetes mellitus is estimated to increase to 439 million affected adults worldwide by 2030 [2]. The diabetes epidemic will necessitate progressive approaches to care of the disease and its complications. Early detection, accurate diagnosis, and timely treatment of visionthreatening diabetic retinopathy have long been established as a means to significantly reduce vision loss from diabetes and improve population health. Multiple professional organizations, including the American Academy of Ophthalmology, recognize the minimum requirement of an annual retinal evaluation for patients with diabetes. Despite these
recommendations, a substantial proportion of patients with diabetes worldwide still do not receive recommended eye care. In the USA, only approximately half of the diagnosed population with diabetes is screened annually for diabetic retinopathy, perpetuating little change over several decades [3]. Vision loss and greater healthcare and societal costs result when patients with diabetes present for eye
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Wilmer Eye Institute, Johns Hopkins University Medical Institutions, Baltimore, Maryland, bDepartment of Ophthalmology, University of Colorado Health Sciences Center, Anschutz Medical Campus, Aurora, Colorado, USA and cRetina Specialty Institute, Pensacola, FL, USA Correspondence to Ingrid E. Zimmer-Galler, MD, Wilmer Eye Institute, Johns Hopkins University Medical Institutions, 600 N Wolfe Street, Maumenee 738, Baltimore, MD 21287, USA. Tel: +1 301 620 9268; e-mail: [email protected] Curr Opin Ophthalmol 2015, 26:167–172 DOI:10.1097/ICU.0000000000000142
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KEY POINTS Telemedicine applications may be utilized to increase diabetic retinopathy assessment rates and may decrease vision loss from diabetic eye disease. New imaging technologies, such as wide-field imaging and optical coherence tomography, may provide additional benefits for telemedicine identification of diabetic retinopathy, but the cost may preclude widespread use. Financial factors remain a major challenge for long-term viability and widespread implementation of telemedicine diabetic retinopathy programs in the USA.
outlining essential components including a robust technology platform, quality assurance procedures, efficient workflows, cost–effectiveness and adequate reimbursement, as well as compliance with legal and regulatory requirements [6]. Rigorous validation to ensure the program meets evidence-based standards of care is essential [6,7]. Over the past decade, many telemedicine diabetic retinopathy programs have published their validation studies demonstrating various successful aspects of the technology, including quality of remotely acquired retinal images, accuracy of remote diagnosis, and early increases in rates of screening for diabetic retinopathy. The overall diagnostic accuracy of telemedicine diabetic retinopathy screening is high, with sensitivity exceeding 80% and specificity of 90% or greater in most published studies [8 ]. Only recently, however, are actual outcomes data becoming available from wide-scale deployments of this technology. This review will explore the current state of telemedicine for diabetic retinopathy assessment, with an emphasis on recent developments and future directions. &
care late in the disease course with delayed diagnosis of a treatable condition. Telemedicine is a striking example of the disruptive innovation required to improve upon key aspects of the healthcare system [4]. Acquisition of retinal images at the point of care in primary care locations outside of the traditional eye care arena can improve patients’ care experience. Remote imaging to detect possible vision-threatening pathology in patients with diabetes, who may be asymptomatic, bridges many barriers such as transportation, concern with pupillary dilation and poor adherence to recommendations for eye evaluations. Reducing the cost of care remains an enduring policy objective in healthcare. The Affordable Care Act of 2010 expands insurance and begins to experiment with new healthcare delivery and financing models [5]. Medicare, Medicaid, and private insurers must create a sustainable financial model for innovations like tele-ophthalmology. Cost avoidance should also be considered in the economic analysis since early detection and treatment resulting from telemedicine diabetic retinopathy screening may generate significant savings in the long term by minimizing progression to late-presenting advanced disease. The use of telemedicine with remote retinal imaging has been shown to be possible across a broad range of populations and geographic areas. Various approaches to teleretinal screening include mydriatic versus nonmydriatic imaging, single field or multiple field imaging, stereoscopic versus monoscopic imaging, and variable threshold levels of diabetic retinopathy dictating when referral is necessary. A tailored approach to the development and implementation of an effective telemedicine diabetic retinopathy assessment program is necessary and is dictated by the program’s goals and objectives. The American Telemedicine Association has published guidelines 168
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CURRENT STATUS OF TELEMEDICINE FOR DIABETIC RETINOPATHY In 2005, the Department of Veterans Affairs instituted what is now the largest telemedicine diabetic retinopathy assessment program implemented in the USA. It is estimated that 90% of the Veterans with diabetes currently undergo an annual evaluation for diabetic retinopathy [9 ]. Kirkizlar et al. [10 ] performed a retrospective random review of 900 Veterans Affairs medical records from a cohort of approximately 9000. Trends by year, for 5 years after implementation of the diabetic retinopathy screening program, were evaluated and showed increasing screening rates, decreasing age of patients undergoing screening, increasing percentage of non-Caucasians receiving screening, and decreased average number of miles traveled for screening. This provides further evidence that large-scale telemedicine programs have a role in increasing adherence to recommended evaluations and in increasing access for different patient populations. Additional information from the Veterans Affairs teleretinal screening program describes the effect of community-based diabetic retinopathy assessment on eye care use and medical center resources. Data from almost 2000 diabetic retinopathy screening events at one Veterans Affairs center over a 6-month period were used to calculate use ratios which may be useful to predict the added resources needed to care for newly referred patients from diabetic retinopathy screening programs [9 ]. &
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Telemedicine diabetic retinopathy screening Zimmer-Galler et al.
The results from the Veterans Affairs teleretinal program alleviate concerns that remote retinal imaging programs may divert patients away from traditional eye care settings. While the task of evaluating all patients with diabetes for the presence of diabetic retinopathy is enormous, there is no evidence to date that telemedicine diabetic retinopathy programs will result in unmanageable referral rates. The Scottish National Diabetic Retinopathy Screening Program has reviewed referral rates over the first 5 years after program introduction in 2006 [11 ]. Out of a total of 225 442 patients eligible for screening for diabetic retinopathy, 187 822 (83.3%) were imaged at least once. There were 560 362 screening episodes during the 5-year study period. Referral rates were greatest in the first 2 years of the program and then remained steady for the following 3 years. This suggests that within 2 years of implementation, the program successfully screened most persons who were previously not evaluated. Referable disease was more commonly found at an individual’s initial screening evaluation and, after the initial increase in referrals, rates stabilized. The most successful telemedicine diabetic retinopathy assessment program in terms of sheer volume is the UK National Health Service Diabetic Eye Screening Program, which now annually assesses almost 2 million patients with diabetes. In an exciting development, Liew et al. [12 ] compared blindness certifications in England and Wales between 1999–2000 and 2009–2010. The leading cause of blindness, out of 1637 certifications received between 1999 and 2000, was diabetic retinopathy. A decade later, the leading cause of blindness, out of 1756 certifications, was hereditary retinal disorders. They concluded, ‘For the first time in at least five decades, diabetic retinopathy/maculopathy is no longer the leading cause of certifiable blindness among working age adults in England and Wales’. They postulate that this change is at least in part related to introduction of nationwide diabetic retinopathy screening programs. A major limitation of this study is that blindness certifications in the United Kingdom are not compulsory and perhaps not all eligible patients were registered as blind. Nonetheless, this is a powerful information indicating for the first time that longterm and wide-scale diabetic retinopathy screening may have an impact on actually reducing vision loss in a large population. &
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ADVANCES IN OCULAR TELEMEDICINE TECHNOLOGY Early Treatment Diabetic Retinopathy Study (ETDRS) 7-field stereo photography (currently performed with digital imaging rather than film) remains the gold standard for detection of diabetic retinopathy and
clinically significant macular edema, and is also the standard against which most diabetic retinopathy screening programs are validated [13]. ETDRS fundus photography is not suitable as a screening tool because it requires an expert photographer and pupil dilation, is time-consuming, and is not efficient for screening purposes. Most screening diabetic retinopathy programs therefore have modified imaging protocols including only one or a few posterior retinal fields. New information suggests that these protocols may be missing significant diabetic pathology. The development of nonmydriatic wide-field cameras may offer an opportunity to optimize photography for diabetic retinopathy screening. With the use of scanning laser ophthalmoscopy (SLO), nonmydriatic imaging covering 180–200 degrees of the retina is possible and has demonstrated significant utility for enhanced diagnosis, treatment, and monitoring of retinal disease. Several investigators have reported on substantial agreement between wide-field SLO and mydriatic 7-field fundus photography for grading diabetic retinopathy [14,15,16 ,17 ]. Silva et al. [18 ] found that one-third of hemorrhages, microaneurysms, intraretinal microvascular abnormalities, and neovascularization were localized outside the coverage area of the ETDRS fields, which resulted in a more severe diabetic retinopathy grade in 10% of the cases. Furthermore, nonmydriatic SLO imaging is technically easy to perform by office staff without expertise. It has also been shown to significantly reduce the unreadable image rate to less than 3% and reduce image evaluation time by 28% when compared with standard fundus photography [19 ]. At present, the main deterrent to large-scale deployment of SLO technology in primary care settings is the substantial cost of the devices, which currently exceeds US $60 000. Investigators from the UK screening program evaluated incorporation of optical coherence tomography (OCT) in addition to retinal photography for patients with surrogate markers for macular edema such as hard exudates [20]. Within the UK program, selective addition of OCT to the screening pathway was cost effective by improving detection of macular edema. The addition of OCT technology to diabetic retinopathy screening programs needs further investigation, but in other healthcare systems, such as in the USA, the additional equipment costs may be prohibitive for screening purposes. &&
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CHALLENGES FOR TELEMEDICINE DIABETIC RETINOPATHY PROGRAMS: FINANCIAL FACTORS In the USA, the Veterans Affairs (and Indian Health Service) telemedicine diabetic retinopathy programs
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are funded by recurring federal appropriations. Many additional diabetic retinopathy screening programs were initially established with grant support, but ultimately proved to not be financially viable for ongoing clinical operation after funding was exhausted. Few large private telemedicine diabetic retinopathy programs have been successful in the long term in the USA because financial sustainability remains a major challenge without additional funding sources. Several different business models for telemedicine diabetic retinopathy programs exist. The most common arrangement utilizes the primary care arena as the point of service where retinal images are acquired. The images and patient demographics are transmitted to a remote reading center for expert assessment and a report is returned to the primary care provider detailing whether referral to an ophthalmologist is necessary. The retinal camera may be purchased or leased by the primary care physician who has an agreement with a reading center for image interpretation. Reimbursement is usually divided into image capture (technical) and image interpretation (professional) components for the primary care office and reading center, respectively. Computing and telecommunications costs are no longer a barrier, and broad bandwidth is almost universally available and inexpensive. However, retinal cameras continue to approach US $15 000 to US $20 000 including installation and servicing which is often too costly for individual primary care offices with limited numbers of patients with diabetes. Research and development has been ongoing for over a decade, but a true low-cost (less than US $1000) validated nonmydriatic retinal camera is still not available. An interesting area of study is the use of smartphone technology as an inexpensive fundus camera. Many technical issues remain and currently there are no validated smartphone camera systems in use with image quality adequate for teleretinal screening, but the possibility of an inexpensive, widely available, portable, and wireless imaging platform is intriguing [21 ,22 ]. Studies on the cost–effectiveness of the Veterans Affairs and UK telemedicine diabetic retinopathy programs have been performed, but these results are not directly applicable to programs being implemented in community primary care settings in the USA [9 ,20]. Limited current information on the cost effectiveness of diabetic retinopathy screening in community settings in the USA is available in the literature. The costs of screening can vary considerably. In one community-based program for disadvantaged patients, the cost of screening per patient was estimated to be US $100 [23]. In the first 18 months after implementation, Harris Health &
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System in Houston, Texas, in collaboration with a commercially available telemedicine diabetic retinopathy assessment program (Intelligent Retinal Imaging Systems, Pensacola, Florida, USA), was able to achieve an increase in diabetic retinopathy screening rates from 62 to 86% in a population of 48 000 patients with diabetes. The screening cost per patient was calculated to be less than US $50 for the 27 302 unique patients screened [24]. Not only is reimbursement for telemedicine diabetic retinopathy services not adequate to cover these costs, it presents a very confusing landscape at present. Traditionally, Current Procedural Terminology (CPT) code 92 250 for fundus photography was used to bill for diabetic retinopathy telemedicine services. In 2011, new remote retinal imaging CPT codes 92 227 and 92 228 were introduced. However, these codes are difficult to use as they do not adequately describe the work being performed by most telemedicine programs and they do not adequately cover the costs associated with teleretinal screening. The descriptor for CPT code 92 227 is remote imaging for detection of retinal disease under physician supervision, which implies that a nonlicensed provider interprets the images. The reimbursement is very low (less than US $15) because there is no compensation for physician work. The descriptor for CPT code 92 228 is remote imaging for monitoring and management of active retinal disease with physician review, interpretation and report. While reimbursement is somewhat higher (less than US $40), CPT code 92 228 can only be used for patients in whom diabetic retinopathy, or active disease, is present, which is generally a minority of the patients being screened. Furthermore, there are inconsistent coverage policies among Medicare carriers, and often neither of the two remote retinal imaging codes is covered. The lack of adequate reimbursement for telemedicine diabetic retinopathy assessment continues to be a major barrier to widespread implementation. Some of the current prohibitive financial barriers for implementation of diabetic retinopathy telemedicine programs may be mitigated in the future as pay-for-performance and penalties for missing key quality measures become more substantial. However, incorporating new and more expensive imaging technology into diabetic retinopathy assessment programs will further complicate the financial sustainability of these programs.
QUALITY ASSURANCE AND CONTROL In order to achieve the highest possible standards, quality metrics are an integral component of a telemedicine diabetic retinopathy assessment program. Volume 26 Number 3 May 2015
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Telemedicine diabetic retinopathy screening Zimmer-Galler et al.
Quality assurance focuses on continuously assessing performance, whereas quality improvement focuses on enhancing performance. Ocular telehealth programs should have protocols in place to monitor and evaluate performance of all components of the program, including assessment rates, gradeability of images, quality of grading, timeliness of reports, and follow-up of screen-positive patients. Continued education and certification of persons acquiring images, as well as graders, should be emphasized in addition to adherence to established protocols. Whereas the United Kingdom has quality standards and key performance indicators in place, further investigation is needed to establish uniform quality metrics for diabetic retinopathy screening programs in the USA [25].
FUTURE DIRECTIONS To address the impact on healthcare resources from the expected global increase in the diabetes population, automation of retinal image evaluation by using computers to either assist or fully automate diabetic retinopathy evaluation will be a critical step in helping to decrease the burden of manual retinopathy evaluation while still providing quality eye care. Ultimately, automated retinal image analysis will be necessary to increase the efficiency of image grading in a cost-effective manner. The field is evolving rapidly, but at present there are no automated retinal image analysis algorithms with United States Food and Drug Administration (FDA) clearance for use in the USA. To date, most research efforts have focused on algorithm development rather than measuring the clinical impact and public health significance of the automated systems. A detailed discussion of the current work with these systems is beyond the scope of this review [26,27,28 ]. In addition to the potential for a smartphonebased fundus camera, a mobile phone-based tele-ophthalmology platform holds significant future promise. New applications and interfaces may augment healthcare delivery by allowing image interpretation, data collection, wireless transfer, and integration into electronic medical records [29]. Utilization of teleretinal technology to detect ocular disease other than diabetic retinopathy is in the early stages, and limited information exists in the literature assessing strategies for grading and detecting additional eye diseases in adults. However, diabetic retinopathy screening programs ultimately need to be powerful enough to identify other abnormalities, suggestive of disease that may lead to vision loss. Additionally, retinal images of some patients obtained through diabetic retinopathy assessment programs will invariably include abnormal findings
other than diabetic retinopathy. Glaucoma and agerelated macular degeneration, in particular, remain important causes of vision loss in the elderly, and the role for telemedicine technology in these diseases is being investigated [30 ,31,32 ]. &
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CONCLUSION The use of an ocular telemedicine approach for diabetic retinopathy assessment has the potential to expand our standard concept of eye care delivery by extending access to care, offering alternative methods for receiving appropriate care and integrating diabetes eye care into the patient’s total healthcare. As Dartmouth professor Batalden states, ‘If we keep doing what we have been doing, we’ll keep getting what we’ve always gotten’ – an expensive and inefficient healthcare system that screens only half of the known population with diabetes [33]. Acknowledgements None. Financial support and sponsorship None. Conflicts of interest S.G. is a consultant for Allergan, Alcon, and Genentech, owns stock/stock options for Intelligent Retinal Imaging Systems and has principal in USRetina.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest
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1. Berwick DM, Nolan TW, Whittington J. The triple aim: care, health and cost. Health Aff (Millwood) 2008; 27:759–769. 2. Shaw J, Sicree R, Zimmet P. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010; 87:4–14. 3. National Committee for Quality Assurance. The state of healthcare quality report 2014. ePub http://ncqa.org. [Accessed 2 December 2014] 4. Christenson CM, Grossman JH, Hwang J. The innovator’s prescription: a disruptive solution for healthcare. McGraw-Hill; 2008; pp. 123–125. 5. The Henry J. Kaiser Family Foundation. Summary of the affordable care act. http://kaiserfamilyfoundation.files.wordpress.com/2011/04/8061-021.pdf. [Accessed 15 December 2014] 6. Li H, Horton M, Bursell S, et al. Telehealth practice recommendations for diabetic retinopathy, second edition. Telemed EHealth 2011; 17:814–837. 7. Williams G, Scott I, Haller J, et al. Single-field fundus photography for diabetic retinopathy screening: a report by the American Academy of Ophthalmology. Ophthalmology 2004; 111:1055–1062. 8. Shi L, Wu H, Dong J, Jiang K, Lu X, Shi J. Telemedicine for detecting diabetic & retinopathy: a systematic review and meta-analysis. Br J Ophthalmol 2015; 1–9. [Epub ahead of print] This meta-analysis includes 20 publications and determined that diagnostic accuracy of telemedicine diabetic retinopathy detection is high. Diagnostic accuracy was higher for images obtained with mydriasis and with wide-field imaging. 9. Chasan J, DeLaune B, Maa A, Lynch M. Effect of a tele retinal screening & program on eye care use and resources. J Am Med Assoc Ophthalmol 2014; 132:1045–1051. This study evaluates measurable resource burdens to be anticipated from increased volume of clinical care as a result of implementation of a telemedicine diabetic retinopathy screening program.
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Retinal, vitreous and macular disorders 10. Kirkizlar E, Serban N, Sisson J, et al. Evaluation of telemedicine for screening of diabetic retinopathy in the Veterans Health Administration. Ophthalmology 2013; 120:2604–2610. Within the Veterans Administration health system, telemedicine diabetic retinopathy screening was found to be cost effective for patient populations greater than 3500 patients, patients less than 80 years of age, and all racial groups. After implementation of the telemedicine program, the average age of patients being screened decreased and the percentage of non-white patients receiving screenings increased. 11. Looker HC, Nyangoma SO, Cromie DT, Olson JA, Leese GP, Black MW, Doig & J, et al. Scottish Diabetes Research Network Epidemiology Group; Scottish Diabetic Retinopathy Collaborative. Rates of referable eye disease in the Scottish National Diabetic Retinopathy Screening Programme. Br J Ophthalmol 2014; 98:790–795. Referral rates for diabetic retinopathy and maculopathy were evaluated over a 5-year period after implementation of a national diabetic retinopathy screening program in Scotland. The yield of referable disease was greatest in the first two years and then stabilized for subsequent years. Suspected diabetic macular edema was the most common reason for referral. 12. Liew G, Michaelides M, Bunce C. A comparison of the causes of blindness && certifications in England and Wales in working age adults (16–64 years), 1999–2000 with 2009–2010. Br Med J Open 2014; 4:e004015. The leading cause of blindness certifications in England and Wales in 1999–2000 was diabetic retinopathy and maculopathy, whereas in 2009–2010, the leading cause of blindness certifications was hereditary retinal disorders. The fact that diabetic retinopathy is no longer the leading cause of certifiable blindness in England and Wales may be related to introduction of a nationwide diabetic retinopathy screening program as well as improved glycemic control. 13. Early Treatment Diabetic Retinopathy Research Study Group. Grading diabetic retinopathy from stereoscopic color fundus photographs: an extension of the modified Airlie House classification. ETDRS report number 10. Ophthalmology 1991; 98:786–806. 14. Kernt M, Hadi I, Pinter F, et al. Assessment of diabetic retinopathy using nonmydriatic ultra-widefield scanning laser ophthalmoscopy (Optomap) compared with ETDRS 7-field stereo photography. Diabetes Care 2012; 35:2459–2463. 15. Silva P, Cavallerano J, Sun J, et al. Nonmydriatic ultrawide field retinal imaging compared with dilated standard 7-field 35 mm photography and retinal specialist examination for evaluation of diabetic retinopathy. Am J Ophthalmol 2012; 154:549–559. 16. Rasmussen M, Broe R, Frydkjaer-Olsen U, et al. Comparison between Early && Treatment Diabetic Retinopathy Study 7: field retinal photos and nonmydriatic, mydriatic and mydriatic steered wide field scanning laser ophthalmoscopy for assessment of diabetic retinopathy. J Diabetes Complications 2015; 29:99–104. Nonmydriatic wide-field retinal images were compared with and matched favorably with mydriatic seven-field ETDRS photographs for 190 eyes in patients with diabetes mellitus. Overlapping eyelashes and distortion may result in missing some lesions with wide-field images. 17. Liegl R, Liegl K, Ceklic L, et al. Nonmydriatic ultra-wide-field scanning laser & ophthalmoscopy (Optomap) versus two-field fundus photography in diabetic retinopathy. Ophthalmologica 2014; 231:31–36. Nonmydriatic wide-field imaging of 143 eyes was compared with mydriatic twofield fundus photography for diabetic retinopathy grading. Overall correlation for grading diabetic retinopathy level was moderate and correlation was substantial for clinically significant macular edema. 18. Silva P, Cavallerano J, Sun J, et al. Peripheral lesions identified by mydriatic & ultrawide field imaging: distribution and potential impact on diabetic retinopathy severity. Ophthalmology 2013; 120:2587–2595. Mydriatic ultrawide-field imaging was compared with ETDRS seven field photography in 206 eyes. Substantial agreement was noted in determining diabetic retinopathy severity. Additional peripheral lesions were noted with ultrawide-field imaging resulting in more severe assessment of diabetic retinopathy than determined with ETDRS photographs in 10% of patients. &
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19. Silva P, Cavallerano J, Tolls D, et al. Potential efficiency benefits of nonmydriatic ultrawide field retinal imaging in an ocular telehealth diabetic retinopathy program. Diabetes Care 2014; 37:50–55. The efficiency of nonmydriatic fundus photography and nonmydriatic ultrawidefield imaging was compared in an ocular telehealth program. A more severe diabetic retinopathy severity level was suggested in 9% of eyes imaged with the wide-field technique. Additionally, the ungradable rate was reduced by 71% and the image evaluation time was reduced by 28% with ultrawide-field images suggesting improved efficiency of diabetic retinopathy teleretinal screening with wide-field imaging devices. 20. Prescott G, Sharp P, Goatman K, et al. Improving the cost-effectiveness of photographic screening for diabetic macular edema: a prospective, multicentre, UK study. Br J Ophthalmol 2014; 98:1042–1049. 21. Maamari R, Keenan J, Fletcher D, Margolis T. A mobile phone-based retinal & camera for portable wide field imaging. Br J Ophthalmol 2014; 98:438–441. The authors have developed a smart-phone based retinal camera with off-the-shelf components capable of wide-field imaging. A validation study for diabetic retinopathy assessment has not been performed with the camera. 22. Darma S, Zantvoord F, Verbraak FD. The quality and usability of smartphone & and hand-held fundus photography, compared to standard fundus photography. Acta Ophthalmol 2014; doi: 10.1111/aos.12632 [Epub ahead of print] Images from 27 eyes were obtained with a smartphone-assisted device, hand-held fundus photography device and standard fundus camera. Image quality of the smartphone set-up was far less than with standard fundus photography and less than with the hand-held device. 23. Byrne M, Parker D, Tannenbaum S, et al. Cost of a community-based diabetic retinopathy screening program. Diabetes Care 2014; 37:e236–e237. 24. Zimmer-Galler I, Silva P. Proceedings of 32nd Annual Meeting of American Society of Retina Specialists. 9–12 August 2014; San Diego, California. 25. NHS Diabetic Eye Screening Programme. http://diabeticeyescreening.nhs.uk. [Accessed 2 January 2015] 26. Trucco E, Ruggeri A, Karnowski T, et al. Validating retinal fundus image analysis algorithms: issues and a proposal. Invest Ophthalmol Vis Sci 2013; 54:3546–3559. 27. Abramoff M, Folk J, Han D, et al. Automated analysis of retinal images for detection of referable diabetic retinopathy. J Am Med Assoc Ophthalmol 2013; 131:351–357. 28. Abramoff MD, Niemeijer M. Mass screening of diabetic retinopathy using & automated methods. In Teleophthalmology in Preventive Medicine. Michelson G, editor. Berlin Heidelberg: Springer Verlag; 2015. Review of scientific studies of automated methods for mass screening evaluated on at least 300 persons with diabetes reveals they achieve a sensitivity of at least 80%. This suggests that automated methods for mass screening of diabetic eye disease have matured and are now safe to consider deployment in clinical practice. 29. Kumar S, Wang E, Pokabla M, Noecker R. Teleophthalmology assessment of diabetic retinopathy fundus images: smartphone versus standard office computer workstation. Telemed J EHealth 2012; 18:158–162. 30. Verma S, Arora S, Kassam F, et al. Northern Alberta remote tele glaucoma & program: clinical outcomes and patient disposition. Can J Ophthalmol 2014; 49:135–140. This study describes a successful tele-glaucoma program, which stratifies patients based on known risk factors and utilizes equipment in addition to a fundus camera. 31. Kassam F, Amin S, Sogbesan E, Damji K. The use of tele glaucoma at the University of Alberta. J Telemed Telecare 2012; 18:367–373. 32. Li B, Powell A, Hooper P, Sheidow TG. J Am Med Assoc Ophthalmol 2014. & [Epub ahead of print] This study, comparing telemedicine screening and monitoring for neovascular agerelated macular degeneration with retina specialist evaluation, found that telemonitoring results in longer time interval before treatment reinitiation, but does not lead to adverse visual outcomes and may decrease the burden of follow-up visits with retinal specialists. 33. McInnis D. What system? Dartmouth Med 2006;28–35. dartmed.dartmouth.edu.
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