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Rising prevalence of diabetes worldwide has necessitated the implementation of population-based diabetic retinopathy (DR) screening programs that can perform retinal imaging and interpretation for extremely large patient cohorts in a rapid and sensitive manner while minimizing inappropriate referrals to retina specialists. While most current screening programs employ mydriatic or nonmydriatic color fundus photography and trained image graders to identify referable DR, new imaging modalities offer significant improvements in diagnostic accuracy, throughput, and affordability. Smartphone-based fundus photography, macular optical coherence tomography, ultrawide-field imaging, and artificial intelligence-based image reading address limitations of current approaches and will likely become necessary as DR becomes more prevalent. Here we review current trends in imaging for DR screening and emerging technologies that show potential for improving upon current screening approaches.
Cho NH, et al. IDF diabetes atlas. 7th ed. Brussels: International Diabetes Federation; 2015.
Lee R, Wong TY, Sabanayagam C. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vis (Lond). 2015;2:17.
Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010;376(9735):124–36. PubMed
Aiello LP, et al. Diabetic retinopathy. Diabetes Care. 1998;21(1):143–56. PubMed
Group TDRSR. Photocoagulation treatment of proliferative diabetic retinopathy. Clinical application of Diabetic Retinopathy Study (DRS) findings, DRS Report Number 8. The Diabetic Retinopathy Study Research Group. Ophthalmology. 1981;88(7):583–600.
Group TDRSR. Early photocoagulation for diabetic retinopathy. ETDRS report number 9. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology. 1991;98(5 Suppl):766–85.
Ross EL, et al. Cost-effectiveness of aflibercept, bevacizumab, and ranibizumab for diabetic macular edema treatment: analysis from the Diabetic Retinopathy Clinical Research Network Comparative Effectiveness Trial. JAMA Ophthalmol. 2016;134(8):888–96. PubMed
Gangwani RA, et al. Diabetic retinopathy screening: global and local perspective. Hong Kong Med J. 2016;22(5):486–95. PubMed
Stefansson E, et al. Screening and prevention of diabetic blindness. Acta Ophthalmol Scand. 2000;78(4):374–85. PubMed
Lau HC, et al. Mass screening for diabetic retinopathy—a report on diabetic retinal screening in primary care clinics in Singapore. Singap Med J. 1995;36(5):510–3.
Backlund LB, Algvere PV, Rosenqvist U. New blindness in diabetes reduced by more than one-third in Stockholm County. Diabet Med. 1997;14(9):732–40. PubMed
Newcomb PA, Klein R. Factors associated with compliance following diabetic eye screening. J Diabet Complicat. 1990;4(1):8–14.
Wong TY, et al. Guidelines on diabetic eye care: the international council of ophthalmology recommendations for screening, follow-up, referral, and treatment based on resource settings. Ophthalmology. 2018;125(10):1608–22. PubMed
Lian JX, et al. Systematic screening for diabetic retinopathy (DR) in Hong Kong: prevalence of DR and visual impairment among diabetic population. Br J Ophthalmol. 2016;100(2):151–5. PubMed
Prescott G, et al. Improving the cost-effectiveness of photographic screening for diabetic macular oedema: a prospective, multi-centre, UK study. Br J Ophthalmol. 2014;98(8):1042–9. PubMed
Kawasaki R, et al. Cost-utility analysis of screening for diabetic retinopathy in Japan: a probabilistic Markov modeling study. Ophthalmic Epidemiol. 2015;22(1):4–12. PubMed
Rachapelle S, et al. The cost-utility of telemedicine to screen for diabetic retinopathy in India. Ophthalmology. 2013;120(3):566–73. PubMed
Lin DY, et al. The sensitivity and specificity of single-field nonmydriatic monochromatic digital fundus photography with remote image interpretation for diabetic retinopathy screening: a comparison with ophthalmoscopy and standardized mydriatic color photography. Am J Ophthalmol. 2002;134(2):204–13. PubMed
Bernardes R, Serranho P, Lobo C. Digital ocular fundus imaging: a review. Ophthalmologica. 2011;226(4):161–81. PubMed
Li HK, et al. Digital versus film Fundus photography for research grading of diabetic retinopathy severity. Investig Ophthalmol Vis Sci. 2010;51(11):5846–52.
Taylor DJ, et al. Image-quality standardization for diabetic retinopathy screening. Expert Rev Ophthalmol. 2009;4(5):469–76.
Cornsweet T. Pixels in fundus cameras: how many do you need? Int Agency Prev Blindness. 2015(April 3):1–5.
Tyler ME, et al. Characteristics of digital fundus camera system affecting tonal resolution in color retinal images. J Ophthalmic Photo. 2009;31:9–14.
Scanlon PH, et al. The effectiveness of screening for diabetic retinopathy by digital imaging photography and technician ophthalmoscopy. Diabet Med. 2003;20(6):467–74. PubMed
Group ETDRSR. Grading diabetic retinopathy from stereoscopic color fundus photographs—an extension of the modified Airlie House classification. ETDRS report number 10. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology. 1991;98(5 Suppl):786–806.
Zimmer-Galler IE, Zeimer R. Telemedicine in diabetic retinopathy screening. Int Ophthalmol Clin. 2009;49(2):75–86. PubMed
Wharton H, Gibson J, Dodson P. How accurate are photographic surrogate markers used to detect macular oedema in the English National Screening Programme? In: Royal College of Ophthalmologists Annual Congress. Birmingham: Royal College of Ophthalmologists; 2011. p. 105.
Wong RL, et al. Are we making good use of our public resources? The false-positive rate of screening by fundus photography for diabetic macular oedema. Hong Kong Med J. 2017;23(4):356–64. PubMed
Wang YT, et al. Comparison of prevalence of diabetic macular edema based on monocular fundus photography vs optical coherence tomography. JAMA Ophthalmol. 2016;134(2):222–8. PubMed
O’Halloran RA, Turner AW. Evaluating the impact of optical coherence tomography in diabetic retinopathy screening for an aboriginal population. Clin Exp Ophthalmol. 2018;46(2):116–21. PubMed
Nguyen HV, et al. Cost-effectiveness of a National Telemedicine Diabetic Retinopathy Screening Program in Singapore. Ophthalmology. 2016;123(12):2571–80. PubMed
Bhargava M, et al. Accuracy of diabetic retinopathy screening by trained non-physician graders using non-mydriatic fundus camera. Singap Med J. 2012;53(11):715–9.
McKenna M, et al. Accuracy of trained rural ophthalmologists versus non-medical image graders in the diagnosis of diabetic retinopathy in rural China. Br J Ophthalmol. 2018;102:1471–6. PubMed
Deb N, et al. Screening for diabetic retinopathy in France. Diabetes Metab. 2004;30(2):140–5. PubMed
Owens DR, et al. Screening for diabetic retinopathy. Diabet Med. 1991;8:S4–10. PubMed
Gulshan V, et al. Development and validation of a deep learning algorithm for detection of diabetic retinopathy in retinal fundus photographs. JAMA. 2016;316(22):2402–10. PubMed
Gargeya R, Leng T. Automated identification of diabetic retinopathy using deep learning. Ophthalmology. 2017;124(7):962–9. PubMed
Li Z, et al. Efficacy of a deep learning system for detecting glaucomatous optic neuropathy based on color fundus photographs. Ophthalmology. 2018;125(8):1199–1206. PubMed
Abramoff MD, et al. Improved automated detection of diabetic retinopathy on a publicly available dataset through integration of deep learning. Investig Ophthalmol Vis Sci. 2016;57(13):5200–6.
Krause J, et al. Grader variability and the importance of reference standards for evaluating machine learning models for diabetic retinopathy. Ophthalmology. 2018;125(8):1264–72. PubMed
De Fauw J, et al. Clinically applicable deep learning for diagnosis and referral in retinal disease. Nat Med. 2018;24:1342–50. PubMed
van der Heijden AA, et al. Validation of automated screening for referable diabetic retinopathy with the IDx-DR device in the Hoorn Diabetes Care System. Acta Ophthalmol. 2018;96(1):63–8. PubMed
Lynch SK, et al. Catastrophic failure in image-based convolutional neural network algorithms for detecting diabetic retinopathy. Investig Ophthalmol Vis Sci. 2017;58:3776.
Silva PS, et al. Peripheral lesions identified on ultrawide field imaging predict increased risk of diabetic retinopathy progression over 4 years. Ophthalmology. 2015;122(5):949–56. PubMed
Silva PS, et al. Diabetic retinopathy severity and peripheral lesions are associated with nonperfusion on ultrawide field angiography. Ophthalmology. 2015;122(12):2465–72. PubMed
Silva PS, 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(3):549–59. PubMed
Wessel MM, et al. Ultra-wide-field angiography improves the detection and classification of diabetic retinopathy. Retina. 2012;32(4):785–91. PubMed
Silva PS, et al. Hemorrhage and/or microaneurysm severity and count in ultrawide field images and early treatment diabetic retinopathy study photography. Ophthalmology. 2017;124(7):970–6. PubMed
Silva PS, et al. Identification of diabetic retinopathy and ungradable image rate with ultrawide field imaging in a National Teleophthalmology Program. Ophthalmology. 2016;123(6):1360–7. PubMed
Hackenthal V. New scan for diabetic eye disease is better, but at a cost. In: Medscape ophthalmology. National Libraries of Medicine. 2016.
Tan ACS, et al. An overview of the clinical applications of optical coherence tomography angiography. Eye (Lond). 2018;32(2):262–86.
Spaide RF, et al. Optical coherence tomography angiography. Prog Retin Eye Res. 2018;64:1–55. PubMed
Krawitz BD, et al. Acircularity index and axis ratio of the foveal avascular zone in diabetic eyes and healthy controls measured by optical coherence tomography angiography. Vis Res. 2017;139:177–86. PubMed
Agemy SA, et al. Retinal vascular perfusion density mapping using optical coherence tomography angiography in normals and diabetic retinopathy patients. Retina. 2015;35(11):2353–63. PubMed
Ting DSW, et al. Optical coherence tomographic angiography in type 2 diabetes and diabetic retinopathy. JAMA Ophthalmol. 2017;135(4):306–12. PubMed
Samara WA, et al. Quantification of diabetic macular ischemia using optical coherence tomography angiography and its relationship with visual acuity. Ophthalmology. 2017;124(2):235–44. PubMed
Lord RK, et al. Novel uses of smartphones in ophthalmology. Ophthalmology. 2010;117(6):1274e3.
Tan GS, et al. Is routine pupil dilation safe among asian patients with diabetes? Investig Ophthalmol Vis Sci. 2009;50(9):4110–3.
Toy BC, et al. Smartphone-based dilated fundus photography and near visual acuity testing as inexpensive screening tools to detect referral warranted diabetic eye disease. Retina. 2016;36(5):1000–8. PubMed
Russo A, et al. Comparison of smartphone ophthalmoscopy with slit-lamp biomicroscopy for grading diabetic retinopathy. Am J Ophthalmol. 2015;159(2):360–4. PubMed
Wadhwani M, et al. Diabetic retinopathy screening programme utilising non-mydriatic fundus imaging in slum populations of New Delhi, India. Trop Med Int Health. 2018;23(4):405–14. PubMed
Sengupta S, et al. Screening for vision-threatening diabetic retinopathy in South India: comparing portable non-mydriatic and standard fundus cameras and clinical exam. Eye (Lond). 2018;32(2):375–83.
Sharma A. Emerging simplified retinal imaging. Dev Ophthalmol. 2017;60:56–62. PubMed
Matimba A, et al. Tele-ophthalmology: opportunities for improving diabetes eye care in resource- and specialist-limited Sub-Saharan African countries. J Telemed Telecare. 2016;22(5):311–6. PubMed
Rajalakshmi R, et al. Automated diabetic retinopathy detection in smartphone-based fundus photography using artificial intelligence. Eye (Lond). 2018;32(6):1138–44.
Pieczynski J, Grzybowski A. Review of diabetic retinopathy screening methods and programmes adopted in different parts of the world. Eur Ophthal Rev. 2015;9(1):49–55.
Tozer K, Woodward MA, Newman-Casey PA. Telemedicine and diabetic retinopathy: review of published screening programs. J Endocrinol Diabetes. 2015;2(4):1–10.
Li HK, et al. Telehealth practice recommendations for diabetic retinopathy, second edition. Telemed J E-Health. 2011;17(10):814–37. PubMed
Zimmer-Galler I, Zeimer R. Results of implementation of the DigiScope for diabetic retinopathy assessment in the primary care environment. Telemed J E Health. 2006;12(2):89–98. PubMed
Massin P, et al. OPHDIAT: a telemedical network screening system for diabetic retinopathy in the Ile-de-France. Diabetes Metab. 2008;34(3):227–34. PubMed
Schulze-Dobold C, et al. Ophdiat((R)): five-year experience of a telemedical screening programme for diabetic retinopathy in Paris and the surrounding area. Diabetes Metab. 2012;38(5):450–7. PubMed
Abramoff MD, Suttorp-Schulten MS. Web-based screening for diabetic retinopathy in a primary care population: the EyeCheck project. Telemed J E Health. 2005;11(6):668–74. PubMed
Sampson CJ, et al. Stratifying the NHS Diabetic Eye Screening Programme: into the unknown? Diabet Med. 2016;33(12):1612–4. PubMed
Sanchez CR, et al. Ocular telemedicine for diabetic retinopathy and the Joslin Vision Network. Semin Ophthalmol. 2010;25(5–6):218–24. PubMed
Aiello LM, et al. Joslin Vision Network Validation Study: pilot image stabilization phase. J Am Optom Assoc. 1998;69(11):699–710. PubMed
Lim MC, et al. Diabetic retinopathy in diabetics referred to a tertiary centre from a nationwide screening programme. Ann Acad Med Singap. 2008;37(9):753–9. PubMed
Nathoo N, et al. The prevalence of diabetic retinopathy as identified by teleophthalmology in rural Alberta. Can J Ophthalmol. 2010;45(1):28–32. PubMed
Ting DS, Tay-Kearney ML, Kanagasingam Y. Light and portable novel device for diabetic retinopathy screening. Clin Exp Ophthalmol. 2012;40(1):e40–6. PubMed
Zhang W, et al. Screening for diabetic retinopathy using a portable, noncontact, nonmydriatic handheld retinal camera. J Diabetes Sci Technol. 2017;11(1):128–34. PubMed
- Advances in Retinal Imaging and Applications in Diabetic Retinopathy Screening: A Review
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- Springer Healthcare
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