noncompliance have included developing comprehensive registries of diabetics, increasing education about the importance of screening, and increased efforts to specifically target underscreened subgroups.10 Especially in regions underserved by eye care professionals, dilated examination by ophthalmologists is increasingly reserved for patients prescreened by digital photographic means and found to have an increased prior probability of sightthreatening retinopathy that would justify this valuable but expensive encounter.

14.24Accountability of Screening Programs

The ultimate goal of screening programs for diabetic retinopathy is to reduce the incidence of visual loss. Provision must be made to determine if progress toward such a goal is being made.95 This involves determination of local statistics on incidence of visual impairment and periodic audits to compare performance over time.95 At its simplest level, these statistics may be incidence of blindness for the population and for the diabetic population. National statistics are too general to be useful given the regional variation in incidence rates of diabetes based on ethnicity, socioeconomic status, and other variables. In Great Britain, the minimum 5-year target is a 10% reduction in incidence of blindness, and an achievable target is 40%.95

14.25 Summary of Key Points

Direct ophthalmoscopy through an undilated pupil by primary health-care providers is insensitive and nonspecific for detecting and classifying DR. Although with training, the performance of this method can improve to acceptable levels for screening purposes, this seems an unattainable goal as a practical matter.

Dilated examination by ophthalmologists and optometrists competent to the task is an impractical screening goal because of poor rates of compliance by the target population of diabetics.

Although screening methods aim for a sensitivity of at least 80% in the detection of diabetic retinopathy, modeling studies suggest that the impact both on years of sight saved and socioeconomic costs levels off for screening methods with sensitivities above 60%.

Single-field nonmydriatic fundus photography is superior to dilated ophthalmoscopy by an ophthalmologist as a screening technique for DR. Referable cases from photographic screening then receive a focused dilated eye examination that accomplishes more than screening – education, detection of nondiabetic eye disease, and assessment for treatment.

Mydriasis decreases the technical failure rate in photoscreening, but does not appreciably increase sensitivity or specificity for detection of DR.

Multiple field fundus photography does not appreciably increase sensitivity or specificity in detecting DR compared to single-field fundus photography.

Balancing all constraints, single-field nonmydriatic fundus photography appears to be the best initial screening method with single-field mydriatic fundus photography for patients with poor dilation such as the elderly.

The ultimate goal of all methods of screening is to place the patient with DR under the care of an ophthalmologist competent to assess the disease status and implement the indicated treatment.

14.26 Future Directions

Better algorithms for automated interpretation of fundus images may reduce the cost of screening by reducing labor costs. Nonmydriatic scanning laser ophthalmoscopic imaging of the fundus may be used in lieu of dilated funduscopy in developed nations, especially by optometrists. Sensitivity and specificity for more than mild DR were 94 and 100%, respectively, compared to ophthalmologist clinical dilated examination gradings in the only study published so far, but only 51 eyes were examined.97 Sensitivity and specificity for CSME were 89–93% and 72–89%, respectively.97 The rate of ungradable images was 9.8%.97 Further studies will need to be done to determine the usefulness of this screening

method. The use of electronic medical records may permit improved communication between primary care physicians and eye care providers to allow detection of patients who have not been screened for diabetic retinopathy. Economic incentives in a variety of forms may improve screening rates.

References

1.Jekel JF, Elmore JG, Katz DL. Epidemiology, Biostatistics, and Preventive Medicine. 1st ed. Philadelphia: WB Saunders; 1996:216–217.

2.Leiter LA, Barr A, Belanger A, et al. Diabetes screening in Canada (DIASCAN) study. Diabetes Care. 2001;24: 1038–1043.

3.Kuo HK, Hsieh HH, Liu RT. Screening for diabetic retinopathy by one-field, non-mydriatic, 45 degrees digital photography is inadequate. Ophthalmologica. 2005; 219:292–296.

4.Diabetes Control and Complications Trial Research Group. Lifetime benefits and costs of intensive therapy as practiced in the diabetes control and complications trial. JAMA. 1996;276:1409–1415.

5.Lin DY, Blumenkranz MS, Brothers RJ, 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; 134:204–213.

6.Tung TH, Shih HC, Chen SJ, et al. Economic evaluation of screening for diabetic retinopathy among Chinese Type 2 diabetics: a community-based study in Kinmen, Taiwan. J Epidemiol. 2008;18:225–233.

7.Vijan S, Hofer TP, Hayward RA. Cost-utility analysis of screening intervals for diabetic retinopathy in patients with type 2 diabetes mellitus. JAMA. 2000;283:889–896.

8.Chew EY, Benson WR, Boldt HC, et al. Diabetic Retinopathy Preferred Practice Guidelines. San Francisco: American Academy of Ophthalmology; 2003.

9.Liesenfeld B, Kohner E, Piehlmeier W, et al. A telemedicine approach to the screening of diabetic retinopathy: digital fundus photography. Diabetes Care. 2000;23: 345–348.

10.Harvey JN, Craney L, Nagendran S, Ng CS. Towards comprehensive population-based screening for diabetic retinopathy: operation of the North Wales diabetic retinopathy screening programme using a central patient register and various screening methods. J Med Screen. 2006;13:87–92.

11.Boucher MC, Nguyen QT, Angioi K. Mass community screeningfordiabeticretinopathyusinganonmydriaticcamera with telemedicine. Can J Ophthalmol. 2005;40:734–742.

12.Raman R, Rani PK, Rachepalle SR, et al. Prevalence of diabetic retinopathy in India. Sankara Nethralaya diabetic retinopathy epidemiology and molecular genetics study report 2. Ophthalmology. 2009;116:311–318.

13.McKay R, McCarty CA, Taylor HR. Diabetic retinopathy in Victoria, Australia: the visual Impairment Project. Br J Ophthalmol. 2000;84:865–870.

14.RoyMS.EyecareinAfricanAmericanswithtype1Diabetes. The New Jersey 725. Ophthalmology. 2004;111:914–920.

15.Moss SE, Klein R, Klein BE. Factors associated with having eye examinations in persons with diabetes. Arch Fam Med. 1995;4:529–534.

16.Wang F, Javitt J. Eye care for elderly Americans with diabetes mellitus; failure to meet current guidelines. Ophthalmology. 1996;103:1744–1750.

17.Bresnick GH, Mukamel DB, Dickinson JC, Cole DR. A screening approach to the surveillance of patients with diabetes for the presence of vision-threatening retinopathy. Ophthalmology. 2000;107:19–24.

18.Sprafka JM, Fritsche TL, Baker R, et al. Prevalence of undiagnosed eye disease in high-risk diabetic individuals. Arch Intern Med. 1990;150:857–861.

19.Wong KC, Wang Z. Prevalence of type 2 diabetes mellitus of Chinese populations in mainland China, Hong Kong, and Taiwan. Diab Res Clin Pract. 2006;73:126–134.

20.Xie XW, Xu L, Wang YX, Jonas JB. Prevalence and associated factors of diabetic retinopathy. The Beijing Eye Study 2006. Graefes Arch Clin Exp Ophthalmol. 2008;246:1519–1526.

21.Farley TF, Mandava N, Prall FR, Carsky C. Accuracy of primary care clinicians in screening for diabetic retinopathy using single-image retinal photography. Ann Fam Med. 2008;6:428–434.

22.Clark J, Grey R, Lim K, Burns-Cox C. Loss of vision before ophthalmic referral in blind and partially sighted diabetics in Bristol. Br J Ophthalmol. 1994;78:741–744.

23.Bek T, Lund-Andersen H, Hansen AB, et al. The prevalence of diabetic retinopathy in patients with screendetected type 2 diabetes in Denmark: the ADDITION study. Acta Ophthalmologica. 2008;E-pub ahead of print.

24.Deb-Joardar N, Germain N, Thuret G, et al. Screening for diabetic retinopathy by ophthalmologists and endocrinologists with pupillary dilation and a nonmydriatic digital camera. Am J Ophthalmol. 2005;140:814–821.

25.Stefansson E, Bek T, Porta M, et al. Screening and prevention of diabetic blindness. Acta Ophthalmol Scand. 2000;78:374–385.

26.Boucher MC, Desroches G, Garcia-Salinas R, et al. Teleophthalmology screening for diabetic retinopathy through mobile imaging units within Canada. Can J Ophthalmol. 2008;43:658–668.

27.Will JC, German RR, Schurman E, et al. Patient adherence to guidelines for diabetes eye care: results from the Diabetic Eye Disease Follow-up Study. Am J Public Health. 1994;84:1669–1671.

28.Moller F, Hansen M, Sjolie AK. Is one 60 degree fundus photograph sufficient for screening of proliferative diabetic retinopathy? Diabetes Care. 2002;24:2083–2085.

29.Klein R, Klein BEK, Neider MW, et al. Diabetic retinopathy as detected using ophthalmoscopy, a nonmydriatic camera and a standard fundus camera. Ophthalmology. 1985;92:486–491.

30.Barrie T, MacCuish AC. Assessment of non-mydriatic fundus photography in detection of diabetic retinopathy. BMJ. 1986;293:1304–1305.

31.von Wendt G, Summanen P, Hallnais K, et al. Detection of diabetic retinopathy: a comparison between red-free digital images and colour transparencies. Graefes Arch Clin Exp Ophthalmol. 2005;243:427–432.

32.James M, Turner DA, Broadbent DM, et al. Cost effectiveness analysis of screening for sight threatening diabetic eye disease. BMJ. 2000;320:1627–1631.

33.Leese GP, Boyle P, Feng Z, et al. Screening uptake in a well-established diabetic retinopathy screening program: the role of geographical access and deprivation. Diabetes Care. 2008;31:2131–2135.

34.Singer DE, Nathan DM, Fogel HA, Schachat AP. Screening for diabetic retinopathy. Ann Intern Med. 1992; 116:660–671.

35.Nathan DM, Fogel HA, Godine JE, et al. Role of the diabetologist in evaluating diabetic retinopathy. Diabetes Care. 1991;14:26–33.

36.Stellingwerf C, Hardus PLLJ, Hooymans MM. Assessing diabetic retinopathy using two-field digital photography and the influence of JPEG-compression. Doc Ophthalmol. 2004;108:203–209.

37.Klein R, Klein BEK, Moss SE, Cruikshanks KJ. The Wisconsin epidemiologic study of diabetic retinopathy. XIV. Ten-year incidence and progression of diabetic retinopathy. Arch Ophthalmol. 1994;112:1217–1228.

38.Klein R, Klein BEK, Moss SE, et al. The Wisconsin epidemiologic study of diabetic retinopathy. II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol. 1984;102:520–526.

39.Lueder GT, Silverstein J, Section on Ophthalmology, et al. Screening for retinopathy in the pediatric patient with type 1 diabetes mellitus. Pediatrics. 2005;116:270–273.

40.Lueder GT, Pradhan S, White NH. Risk of retinopathy in children with type 1 diabetes mellitus before 2 years of age. Am J Ophthalmol. 2005;140:930–931.

41.Scanlon PH, Foy C, Chen FK. Visual acuity measurement and ocular co-morbidity in diabetic retinopathy screening. Br J Ophthalmol. 2008;92:775–778.

42.Anderson S, Broadbent DM, Swain JYS, et al. Ambulatory photographic screening for diabetic retinopathy in nursing homes. Eye. 2003;17:711–716.

43.Trautner C, Icks A, Haastert B, et al. Incidence of blindness in relation to diabetes. Diabetes Care. 1997;20:1147–1153.

44.Sussman E, Tsiaras W, Soper K. Diagnosis of diabetic eye disease. JAMA. 1982;247:3231–3234.

45.O’Hare JP, Hopper A, Madhaven C, et al. Adding retinal photography to screening for diabetic retinopathy: a prospective study in primary care. BMJ. 1996;312:679–682.

46.Davies R, Sullivan P, Canning C. Simulation of diabetic eye disease to compare screening policies. Br J Ophthalmol. 1996;80:945–950.

47.Pugh JA, Jacobson JM, Van Heuven WA, et al. Screening for diabetic retinopathy. The wide angle retinal camera. Diabetes Care. 1993;16:889–895.

48.Harding SP, Broadbent DM, Neoh C, et al. Sensitivity and specificity of photography and direct ophthalmoscopy in screening for sight threatening eye disease: the Liverpool Diabetic Eye Study. BMJ. 1995;311:1131–1135.

49.Moss SA, Klein R, Kessler SD, Richie KA. Comparison between ophthalmoscopy and fundus photography in

determining severity of diabetic retinopathy. Ophthalmology. 1985;92:62–67.

50.Swanson M. Retinopathy screening in individuals with type 2 diabetes: who, how, how often, and at what cost – an epidemiologic review. Optometry. J Am Optom Assoc. 2005;76:636–646.

51.Kleinstein RN, Roseman JM, Herman WH, et al. Detection of diabetic retinopathy by optometrists. J Am Optom Assoc. 1987;58:879–882.

52.Schachat AP, Hyman L, Leke C, et al. Comparison of diabetic retinopathy detection by clinical examinations and photograph gradings. Arch Ophthalmol. 1993;111: 1064–1070.

53.Emanuele N, Klein R, Moritz T, et al. Comparison of dilated fundus examinations with seven-field stereo fundus photographs in the Veterans Affairs Diabetes Trial. J Diabetes Complications. 2008. doi:10.1016/j.jdiacomp. 2008.02.010

54.Kinyoun JL, Martin DC, Fujimoto WY, Leonetti DL. Ophthalmoscopy versus fundus photographs for detecting and grading diabetic retinopathy. Invest Ophthalmol Vis Sci. 1992;33:1888–1893.

55.Williams GA, Scott IU, Haller JA, et al. Single-field fundus photography for diabetic retinopathy screening. A report by the American Academy of Ophthalmology. Ophthalmology. 2004;111:1055–1062.

56.Williams R, Nussey S, Humphrey R, Thompson G. Assessment of non-mydriatic fundus photography in detection of diabetic retinopathy. Br Med J. 1986;293:1140–1142.

57.Browning DJ, McOwen MD, Bowen RM Jr, O’Marah TL. Comparison of the clinical diagnosis of diabetic macular edema with diagnosis by optical coherence tomography. Ophthalmology. 2004;111:712–715.

58.Scott IU, Bressler BN, Bressler SB, et al. Agreement between clinician and reading center gradings of diabetic retinopathy severity level at baseline in a phase 2 study of intravitreal bevacizumab for diabetic macular edema. Retina. 2008;28:36–40.

59.Kinyoun J, Barton FB, Fishner MR, et al. Detection of diabetic macular edema: ophthalmoscopy versus photo- graphy-early treatment diabetic retinopathy study report number 5. Ophthalmology. 1989;96:746–751.

60.McGinn T, Guyatt G, Cook R, Meade M. Diagnosis: measuring agreement beyond chance. In: Guyatt G, Rennie D, eds. User’s Guide to the Medical Literature, 1st ed., Chap. 2C. Chicago: AMA Press; 2002.

61.Murgatroyd H, Ellingford A, Cox A, et al. Effect of mydriasis and different field strategies on digital image screening of diabetic eye disease. Br J Ophthalmol. 2004;88:920–924.

62.Chantelau E, Zwecker M, Weiss H, et al. Fundus polaroid screening for diabetic retinopathy. Is one print per patient enough? Diabetes Care. 1989;12:223–226.

63.Boucher MC, Gresset JA, Angioi K, Olivier S. Effectiveness and safety of screening for diabetic retinopathy with two nonmydriatic digital images compared with the seven standard stereoscopic photographic fields. Can J Ophthalmol. 2003;38:537–542.

64.Beynat J, Charles A, Astruc K, et al. Screening for diabetic retinopathy in a rural French population with a mobile non-mydriatic camera. Diabetes Metab. 2008;35:49–56.

65.The Eye Diseases Prevalence Research Group. The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004;122:552–563.

66.Perrier M, Boucher MC, Angioi K, et al. Comparison of two, three, and four 45 degrees image fields obtained with the Topcon CRW6 nonmydriatic camera for screening for diabetic retinopathy. Can J Ophthalmol. 2003;38: 569–574.

67.Deb-Joarder N, Germain N, Thuret G, et al. Systematic screening for diabetic retinopathy with a digital fundus camera following pupillary dilatation in a university diabetes department. Diabet Med. 2007;24:303–307.

68.Leese GP, Ahmed S, Newton RW, et al. Use of mobile screening unit for diabetic retinopathy in rural and urban areas. BMJ. 1993;306:187–189.

69.Herbert HM, Jordan K, Flanagan DW. Is screening with digital imaging using one retinal view adequate? Eye. 2003;17:497–500.

70.Taylor DJ, Fisher J, Jacob J, Tooke JE. The use of digital cameras in a mobile retinal screening environment. Diabetes Care. 1999;16:680–686.

71.Peters AL, Davidson MB, Ziel FH. Cost-effective screening for diabetic retinopathy using a nonmydriatic retinal camera in a prepaid health-care setting. Diabetes Care. 1993;16:1193–1195.

72.Maberly D, Cruess AF, Barile G, Slakter J. Digital photographic screening for diabetic retinopathy in the James Bay Cree. Ophthalmic Epidemiol. 2002;9: 169–178.

73.Leske MC, Wu SY, Hyman L, et al. Diabetic retinopathy in a black population-the Barbados eye study. Ophthalmology. 1999;106:1893–1899.

74.O’Hare JP, Hopper A, Madhaven C, et al. Adding retinal photography to screening for diabetic retinopathy: a prospective study in primary care. BMJ. 1996;312:679–682.

75.Scanlon PH, Foy C, Malhotra R, Aldington SJ. The influence of age, duration of diabetes, cataract, and pupil size on image quality in digital photographic retinal screening. Diabetes Care. 2005;28:2448–2453.

76.Maberly D, Morris A, Hay D, et al. A comparison of digital retinal image quality among photographers with different levels of training using a nonmydriatic fundus camera. Ophthalmic Epidemiol. 2004;11:191–197.

77.Lim MCC, Lee SY, Cheng BCL, et al. Diabetic retinopathy in diabetics referred to a tertiary center from a nationwide screening program. Ann Acad Med Singapore. 2008;37:753–759.

78.Scanlon PH, Carter S, Foy C, et al. An evaluation of the change in activity and workload arising from diabetic ophthalmology referrals following the introduction of a community based digital retinal photographic screening program. Br J Ophthalmol. 2005;89:971–975.

79.Pandit RJ, Taylor R. Mydriasis and glaucoma: exploding the myth. Diabet Med. 2000;17:693–699.

80.Brown JB, Pedula KL, Summers KH. Diabetic retinopathy. Contemporary prevalence in a well-controlled population. Diabetes Care. 2003;26:2637–2642.

81.Younis N, Broadbent DM, Vora JP, Harding SP. Incidence of sight-threatening retinopathy in patients with type 2 diabetes in the Liverpool Diabetic Eye Study: a cohort study. Lancet. 2003;361:195–200.

82.Lee PP, Meredith LS, Whitcup SM, et al. A comparison of self-reported utilization of ophthalmic care for diabetes in managed care versus fee-for-service. Retina. 1998;18:356–359.

83.The Diabeties Control and Complications Trial Research Group. Color photography vs fluorescein angiography in the detection of diabetic retinopathy in the diabetes control and complications trial. Arch Ophthalmol. 1987;105:1344–1351.

84.Abdel-Ghafar RA, Morris T. Progress towards automated detection and characterization of the optic disc in glaucoma and diabetic retinopathy. Med Inform Internet Med. 2007;32:19–25.

85.Gardner GG, Keating D, Williamson TH, Elliott AT. Automatic detection of diabetic retinopathy using an artificial neural network: a screening tool. Br J Ophthalmol. 1996;80:940–944.

86.Chaum E, Karnowski TP, Govindasamy VP, et al. Automated diagnosis of retinopathy by content-based image retrieval. Retina. 2008;28:1463–1477.

87.JavittJC,AielloLP.Cost-effectivenessofdetectingandtreat- ing diabetic retinopathy. Ann Intern Med. 1996;124:164–169.

88.Dasbach EJ, Fryback DG, Newcomb PA, et al. Costeffectiveness of strategies for detecting diabetic retinopathy. Med Care. 1991;29:20–39.

89.Lairson DR, Pugh JA, Kapadia AS, et al. Cost-effective- ness of alternative methods for diabetic retinopathy screening. Diabetes Care. 1992;15:1369–1377.

90.Fong DS, Gottlieh J, Ferris FL III, Klein R. Understanding the value of diabetic retinopathy screening. Arch Ophthalmol. 2001;119:758–760.

91.Porta M, Bandello F. Diabetic retinopathy. A clinical update. Diabetologia. 2002;45:1617–1634.

92.McCarty CA, Taylor KI, McKay R, et al. Diabetic retinopathy: effects of national guidelines on the referral, examination, and treatment practices of ophthalmologists and optometrists. Clin Exp Ophthalmol. 2001;29:52–58.

93.Diabetes Management Program. Improving multiple aspects of diabetes care. NCQA Website. 2009. 4-4-2009.

94.American College of Physicians ADAaAAoO. Screening Guidelines for Diabetic Retinopathy: clinical Guideline. Ann Intern Med. 1992;116:683–685.

95.Kumar N, Goyder E, McKibbin M. The incidence of visual impairment due to diabetic retinopathy in Leeds. Eye. 2006;20:455–459.

96.Javitt JC, Canner JK, Frank RG, et al. Detecting and treating retinopathy in patients with type 1 diabetes mellitus. Ophthalmology. 1990;97:483–495.

97.Neubauer AS, Kernt M, Haritoglu C, et al. Nonmydriatic screening for diabetic retinopathy by ultra-widefield scanning laser ophthalmoscopy (Optomap). Graefes Arch Clin Exp Ophthalmol. 2008;246:229–235.