Dm
S Y M P O S I U M PROCEEDINGS
Screening for Diabetic Retinopathy D.R. Owens, J. Dolben, S. Young, R.E.J. Ryder, I.R. Jones, T.M. Hayes
J.Vora,
D. Jones, D. Morsman,
Diabetes Research Unit, Department of Medicine, University of Wales College of Medicine, Heath Park, Cardiff, UK
There is a need for greater educational emphasis, both at undergraduate and postgraduate level, on the detection of diabetic eye disease, in particular diabetic retinopathy. The early diagnosis of the sight-threatening lesions of proliferative retinopathy and maculopathy is a prerequisite for the prevention or reduction of the visual loss and blindness associated with this diabetic complication. It i s also essential that patients are aware that diabetes can result in visual loss due to diabetic retinopathy. Patients should understand that diabetic retinopathy may be present without ophthalmic or diabetic symptoms and that its incidence increases with duration of diabetes, poor diabetes control, and hypertension. They must also be aware that, if detected early, retinopathy can be treated successfully and vision preserved. Early detection depends on regular eye examination involving both visual acuity assessment and ophthalmoscopy through dilated pupils by experienced personnel. A comprehensive programme of screening followed by prompt and adequate treatment would made a significant contribution to eradicating diabetic retinopathy as a cause of blindness. KEY WORDS
Diabetic retinopathy Screening Clinical examination Fundus photography
Introduction
efficacy of local treatment with laser photocoagulation, for both proliferative retinopathy and maculopathy is now Long-standing diabetes mellitus results in significant well established and should preferably be instituted diabetic eye disease chiefly affecting the retina (diabetic before the onset of those retinal symptoms associated with retinopathy) and lens (cataract). Diabetic retinopathy is significant visual loss.' 1-14 Photocoagulation produces a a leading cause of blindness in adults between 25 and clear difference in the deterioration rate between treated 74 years of age.14 Up to 98 % of insulin-treated patients and untreated eyes in patients with proliferative retinopadiagnosed before the age of 30 years will have evidence thy. This is especially noticeable in eyes labelled high of diabetic retinopathy after 20 years of diabetes. Sightrisk in whom 50 % of controls and only 15 % of treated threatening proliferative retinopathy may be present in eyes became blind over a 5-year period.",'* In eyes with 50 % of these patients increasing to 67 % after 35 years.5 mild-to-moderate non-proliferative diabetic retinopathy In contrast, up to 20 % of non-insulin-treated patients and macular oedema, deterioration after 3 years occurred have some diabetic retinopathy even at diagn~sis,~,' in 24 % of untreated eyes compared to 12 % of treated increasing to approximately 50 % after a duration of 20 eyes. 3,1 years or more.c1o For the same period of time the Despite these important advances and in view of the prevalence of proliferative retinopathy increases from increasing size of the diabetic population, little or Although the incidence rate of around 5 to 20 no reduction in the overall incidence of new blind retinopathy is two- or three-fold greater amongst Type 1 registrations due to diabetes has yet been achieved.15,16 (insulin-dependent)than Type 2 (non-insulin-dependent) Therefore, the justification and need for retinopathy diabetic patients, the latter is a much larger group and screening in diabetic patients is overwhelming, because contributes over four times more retinopathies. Type 2 it is common, often asymptomatic, and yet eminently diabetic patients represent the major proportion of treatable (especially if detected early). Noteworthy is the diabetic patients requiring ophthalmological care.'O impressive reduction in the rate of blind registration due Proliferative retinopathy is the major occular problem to glaucoma and cataract during the last 20 years which faced by the Type 1 diabetic patient, with maculopathy has been as a direct result of improved medical and the most important for the Type 2 diabetic ~ a t i e n t . ~ , ~ , surgical techniques.' 5 , 1 6 *lo Whereas diabetic retinopathy is rarely a threat to The ability to detect, classify, and quantify diabetic vision during the first 10 years for the Type 1 diabetic retinopathy in a reliable way is necessary if an appropriate patient, this is certainly not the case for the Type 2 management programme is to be chosen for individual diabetic patient with an unknown duration of disease. The patient^.'^ Methods adopted can be divided into those aimed at detecting morphological changes and those which detect functional abnormalities. For morphological changes, considerable advances have been achieved Correspondence to: Dr D.R. Owens, Diabetes Research Unit, Departover the last 20 to 30 years using fundus photography ment of Medicine, University of Wales College of Medicine, Heath Park, Cardiff, UK. in an attempt to classify diabetic retinopathy and grade s4
0742-3071/91/Symposium 0004-07$05.00 & Sons, Ltd.
0 1991 by John Wiley
DIABETIC MEDICINE, 1991; 8 Symposium: S4-S10
nm its severity according to structural The structural abnormalities associated with diabetic retinopathy are usually classified as non-proliferative or proliferative. Non-proliferative diabetic retinopathy refers to intraretinal abnormalities including: microaneurysms, dilated retinal capillaries, retinal haemorrhages, cotton wool spots (ischaemic infarcts), hard exudates, and retinal oedema. These changes can be understood in terms of two underlying and basic pathophysiological processes: retinal vessel closure and abnormal retinal vessel permeability. Proliferative diabetic retinopathy consists of proliferation of fibrovascular and glial tissue in front of the retina; a process thought to be a response to underlying retinal ischaemia. New, (pre-retinal) vessels, at the disc or elsewhere, can cause pre-retinal and vitreous haemorrhage. Vitreous and retinal detachment may result from the shrinkage of the fibrous and glial tissue. Functional abnormalities associated with diabetic retinopathy such as visual acuity, colour vision, perimetry, and contrast sensitivity also lend themselves to q ~ a n t i f i c a t i o n . ~The ~ - ~ presence ~ of functional abnormalities of the retina, and therefore visual disability, may not only indicate the extent of diabetic retinopathy but may precede clinically visible retinopathy and even predict future events. Currently, 1 to 2 % of all diabetic patients are blind or partially sighted14 with between 50 and 70 % of blindness from both proliferative retinopathy and maculopathy being preventable by early detection and treatrnent."-I4 A much larger proportion of patients not registered as blind, but greatly handicapped by visual loss,26 would benefit from an improved level of ophthalmological care. Therefore, it is mandatory to establish an effective screening programme for diabetic eye disease in an attempt to prevent or limit visual loss and blindness from diabetic retinopathy.
SYMPOSIUM PROCEEDINGS conditions which prevail in the majority of busy hospital diabetic and general practitioner clinics, potentially serious misdiagnosis may easily occur and treatable lesions go ~ n d e t e c t e d .It~ has ~ been estimated that up to 10 % of the population attending a diabetic clinic has serious retinopathy, many of whom remain undetected and therefore untreated.33Alternative screening methods therefore need to be considered. At primary care level, screening by ophthalmic opticians in Great Britain confirms their ability to accurately detect abnormalities of the fundus in diabetic patients.34 Their involvement in screening has proved successful in many centres and could be more widely adopted. Evidence from several studies indicates that adequate training is an essential prerequisite for both medical and non-medical personnel involved in detecting diabetic r e t i n ~ p a t h y . ~ ~
Clinical Examination
The first essential step in any screening programme i s to take a detailed history from the patient with special reference to the duration of diabetes and to visual ~ y m p t o m s . As ~ ~ retinopathy may deteriorate during pregnancy, all women with diabetes should, where possible, be examined before the commencement of pregnancy and at 3-monthly intervals throughout the pregnancy. Diabetic patients with hypertension, renal disease or prolonged poor glycaemic control (necessitatinga change in therapy) must also be regarded as at high risk. The assessment of visual acuity remains the mainstay for measuring central retinal and higher order visual function. It is generally carried out using standardized Snellen visual acuity charts, adequately illuminated at a defined distance. One eye is tested at a time and the refractive error corrected if the visual acuity is worse than 6/6 using the patient's spectacles for distance vision. The use of a pinhole card can overcome refractive errors Screening for Diabetic Retinopathy but cannot improve vision. The 'pinhole test' can assist in the differentiation between impaired vision due to The onus to detect and institute treatment for diabetic either refractive error or pathology in the eye. General retinopathy rests with both physician and ophthalmoleye examination follows for the presence of cataract ogist. In any programme of screening it is essential to formation and evidence of rubeosis. The patient is then establish how and when to screen and who should be prepared for fundal examination using a short-acting involved at each stage. Improved education for the mydriatic such as tropicamide (0.5 to 1 %) or phenylephprofessional, patients, and the public is therefore required. rine (2.5 to 10 %). Mydriasis carries a small risk of Ophthalmoscopy by an ophthalmologist aided by precipitating acute glaucoma. Patients known to have fluorescein angiography and colour photography of the glaucoma or having a previous history of eye surgery are fundus affords the most sensitive and specific means best assessed by an ophthalmologist. An efficient working of detecting and assessing diabetic r e t i n ~ p a t h y . ~ ~ ,ophthalmoscope ~~ is a prerequisite for adequate ophthalStereophotography and angiography are both superior to moscopy. ophthalmos~opy with ~ ~ the ~~~ two techniques essentially In diabetic patients diagnosed before the age of 30 of comparable accuracy.3o Under optimal conditions, years, the first retinal examination should occur no later approximately 30 % of physicians with an interest in than 5 years after diagnosis with annual checks from 10 diabetes may fail to diagnose proliferative diabetic years onwards. For patients diagnosed after 30 years of retinopathy by ophthalm~scopy.~'The failure rate can age, retinae should be checked at diagnosis with a increase to an alarming 50 % in the case of more follow-up examination every year. More frequent review junior medical ~ t a f f . ~Therefore, ' under the suboptimal is recommended once lesions of diabetic retinopathy
SCREENING FOR DIABETIC RETINOPATHY
s5
SYMPOSIUM PROCEEDINGS
Dm
are observed. Additional checks are required during pregnancy, and in high-risk patients.
As sight-threatening lesions of diabetic retinopathy may not be detected from Polaroid colour prints obtained with non-mydriatic fundal cameras we conducted a study to compare Polaroid prints in a 'field' situation with Retinal Photography 35 mm colour transparencies (with mydriasis) and fluorIn an attempt to produce a screening procedure that escein angi~grams.~'Eighty-three per cent (105/127) of does not require ophthalmological expertise, various the Polaroid prints were considered assessable compared photographic techniques have been developed. It has to 98 % (124/127) of colour transparencies and 98 % clearly been demonstrated that stereoscopic fundal photo(125/127) of fluorescein angiograms (Table 1). The pickgraphs are more accurate than simple ophthalmoscopic up rate of microaneurysms, haemorrhages, hard exudates, examination,28 with the combination of fluorescein and cotton wool spots was essentially similar for the angiography and colour photographs representing the Polaroid prints and 35 mm transparencies of equivalent most accurate description of retinal m o r p h ~ l o g y . ~ ~ quality (Table 2). Fluorescein angiography revealed a 5 to 8 times greater number of microaneurysms and was Recently the introduction of non-mydriatic 45" cameras superior in detecting new vessels, cotton wool spots, has offered the possibility of large-scale screening without the need for m y d r i a ~ i s . ~The ' ~ ~ Canon CR2-45NM and macular oedema although difficulty in detecting exudative and haemorrhagic lesions was experienced. In (Clement Clark Ltd, London, UK) and Topcon TRC NWtwo cases early disc new vessels were not seen on 2 (Keeler Ltd, London, UK) require a minimal pupil Polaroid prints. The overall detection rate of diabetic diameter of 5 mm and the Canon CR3-NM and Kowa Nonmyd plus (Keeler Ltd, London, UK) cameras a retinopathy in this patient population was 74 % and minimal diameter of 4 mm. Canon CR3-45NM has a 88 % for Polaroid prints and 35 mm transparencies, higher detection rate for diabetic r e t i n ~ p a t h y .The ~~ respectively (Table 3). However, both had limited camera shown in Figure 1 utilizes an infra-red television capacity to demonstrate the presence of preproliferative camera with a suitable filtered light source for viewing and proliferative diabetic retinopathy. the retina as a black and white retinal image on a A more recent study comparing non-mydriatic Polaroid television monitor, while the patient's eye is dark adapted. photography with fundoscopy in 2159 patients rePolaroid colour prints or transparencies obtained using emphasized the potential unreliability of both techniques the Kowa Nonmyd plus and CR3-45NM cameras can be when they are not carried out Under accurate and sensitive for detecting diabetic retinopathy controlled conditions non-mydriatic Polaroid photograin 96.5 % of cases.43Neverthelessan important limitation phy was deemed as good as routine clinic ophthalof the non-mydriatic camera is the restriction to a 45" moscopy through dilated pupils by non-ophthalmologists field, encompassing the disc-macula area. As 8 to 15 % and considerably more reliable for detecting maculopathy of all lesions of diabetic retinopathy and 27 % of cases at a treatable stage. of proliferative diabetic retinopathy reside outside the The rate of usable photographs (10 % were of poor 45" field, the technique is obviously r e ~ t r i c t e d . * ~ , ~ ~quality) ,~~ has been regarded by others to be too low when Although the use of a Polaroid camera makes fundal screening for the sight-threatening lesions of diabetic photographs available with little delay, the resolution of re ti no path^.^^ The potential role of the non-mydriatic camera has to be considered relative to the existing Polaroid film is frequently inadequate to record the presence of small, fine, new vessels with potentially methods of screening available in a variety of different serious consequence^.^!,^^ clinical situations. Its use can be advantageous where the medical staff are either inexperienced or insufficient to deal with the large number of diabetic patients. The camera is potentially useful when used by a trained operator and the prints read by an experienced observer. The observer must be fully aware of the limitations of the procedure and therefore able to decide either to rephotograph with or without mydriasis or refer the patient to an ophthalmologist. The camera is easy to use and provides a reasonably reliable photographic representation of the severity of retinopathy (in broad categories) within its 45" field of vision.39 It is superior to ophthalmoscopy through undilated pupils but cannot be relied upon to detect certain vision-threatening lesions such as macular oedema and early new vessel formation. The potential educational role of non-mydriatic Polaroid retinal photography should not be underestimated when used in parallel with ophthalmoscopy following mydFigure 1. The Canon CR3-4NM non-mydriatic retinal camera riasis. The photographs should assist with and emphasize S6
D.R. OWENS €7 AL.
Dm
SYMPOSIUM PROCEEDINGS Table 1. Quality grading of retinal photographs Quality grade”
Polaroid prints 35 rnrn Transparencies
1
2
3
4
5
60 (47) 116 (91)
45 (35) 8 (6)
18 (14) 2 (2)
4 (3) 1 (1)
0 (0) 0 (0)
Number (%). ’1 = Excellent clarity, 2 = definition of most retinal detail, 3 = limited definition, 4 = gross detail only visible, and 5 = no detail visible.
Table 2. Detection of retinal lesions by three photographic techniques based on assessable photographic records in eyes with diabetic retinopathy (n = 43) Polaroid prints Microaneurysrns Haemorrhages Hard exudates Macular oedema Cotton wool spots IRMA
New vessels
35 rnrn Fluorescein Transparencies angiograrns
5 28 27 2 4 1 0
9 33 26 2 5 0 1
38 19 8 5 12 1 2
IRMA: intraretinal microvascular abnormalities.
the virtues of direct ophthalmoscopy with mydriasis which should eventually make the non-mydriatic camera superfluous to requirements in the context of retinopathy screening. The non-mydriatic camera will not replace proper ophthalmoscopic examination by an experienced attending physician.
Oral fluorescein Fluorescein fundus angiography allows detailed examination of the retinal microcirculation (capillary bed) and retinal blood The presence of cystoid macular oedema, small tufts of new vessels, and leakage from such early neovascularization are clearly demonstrated.
Small haemorrhages and hard exudates may however be less obvious than on a colour p h ~ t o g r a p hThe . ~ ~ use of different filters for colour photography prior to dye injection enables identification and differentiation between exudates, haemorrhages, and retinal pigment defects. The technique of intravenous fluorescein angiography to detect early diabetic retinopathy is at present unsurpassed. However it must be appreciated that this method is associated with unwanted effects in a small proportion of patients. In our recent experience of 100 consecutive Type 2 diabetic patients, 81 had no sideeffects, 15 experienced mild nausea, vomiting occurred in 1, breathlessnesskoughing in 1, and 2 patients had a transient skin rash. This technique is therefore a relatively safe procedure provided the necessary precautions are observed. Orally administered fluorescein has been used by several investigators to circumvent a number of problems associated with the intravenous The procedure is deemed safer and simpler to perform, with better patient acceptance and provides documentation of late dye leakage (Figure 2). Colour photographs are taken between 30 and 60 min following the oral administration of sodium fluorescein in a sweetened drink. In some centres up to 10 % of fluorescein studies are done utilizing the oral which is especially useful in children, patients with difficult veins, and where repeated studies are necessary. The detection and assessment of responses to treatment of retinal vascular leakage especially macular oedema is an obvious area for expansion. It may also be used as an adjunct to Polaroid
Table 3. Comparison of detection rate according to type of retinopathy Diabetic retinopathy
Polaroid prints 35 rnrn Transparency Fluorescein angiogram
All patients
Background
Macular oederna
Preproliferative
Pro1iferative
32 (75) 38 (88) 43 (100)
25 30 26
2 2 3
5 5 12
0 1 2
Number (%). SCREENING FOR DIABETIC RETINOPATHY
s7
Dm
S Y M P O S I U M PROCEEDINGS
Figure 2. Oral fluorescein fundal angiography demonstrating late dye leakage
colour photography of the fundus with non-mydriatic cameras, thereby avoiding failure to detect sight-threatening lesions of cystoid macular oedema and proliferative diabetic retinopathy within a 45" field. Further work is still needed to determine the optimal procedure for this technique.
Conclusions Direct ophthalmoscopy by an experienced observer remains the best method of screening for the presence of diabetic retinopathy. Ophthalmoscopy by non-retinal specialists, through undilated pupils, is an insensitive and non-specific means of detecting or classifying diabetic retinopathy. Clearly there is an urgent need for more education of clinicians in the detection of diabetic eye disease, in particular diabetic retinopathy. The early diagnosis of the sight-threatening lesions of proliferative retinopathy and maculopathy is a prerequisite for the prevention or reduction of the visual loss and blindness associated with diabetic retinopathy. It is also necessary that the patient and the public are made aware that diabetes can result in visual loss. Patient education programmes should encourage an understanding that diabetic retinopathy may be present without ophthalmological symptoms. Patients should also be informed that duration of diabetes, poor diabetes control, and hypertension are associated with a higher incidence of diabetic retinopathy. Pregnancy i s also a time for vigilance. Patients must be aware that retinopathy can be treated successfully and vision preserved provided it is detected early enough. This means regular eye examination involving both visual acuity assessment and
S8
ophthalmoscopy through dilated pupils by experienced personnel. Non-mydriatic cameras have a place in screening for diabetic retinopathy especially where ophthalmological support is limited. Trained operators and experienced readers of the Polaroid prints are essential to avoid failure to diagnose treatable visionthreatening lesions. The cost benefit of the non-mydriatic cameras has to be assessed for each individual situation where diabetic retinopathy screening is considered. The use of oral fluorescein angiography in such screening programmes needs further evaluation. Considerable effort is necessary to initiate and maintain a comprehensive programme of screening for diabetic retinopathy to ensure timely intervention in an attempt to eliminate diabetic retinopathy as a cause of visual loss and blindness in diabetic patients.
Acknowledgements We wish to thank Debra Thomas for typing the manuscript and the Department of Medical Illustration, University Hospital of Wales, for the illustrations.
References Sorsby A. The Incidence and Causes of Blindness in Englandand Wales 1948-1962. Reports on Public Health and Medical Subjects No. 114. London: HMSO, 1966. 2 . Sorsby A. The Incidence and Causes of Blindness in England and Wales 1963-1968. Reports on Public Health and Medical Subjects No. 128. London: HMSO, 1972. 3. Kahn HA, Hiller R. Blindness caused by diabetic retinopa1.
D.R.OWENS E l
AL.
Dm thy. Am J Ophthalmol 1974; 78: 58-67. 4. Ghafour IM, Allen D, Foulds WS. Common causes of blindness and visual handicap in the West of Scotland. Br 1 Ophthalmol 1983; 67: 209-21 3. 5. Klein R, Klein BEK, Moss SE, et al. The Wisconsin Epidemiological Study of Diabetic Retinopathy. I1 Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol 1984; 102: 520-532. 6. Caird FL, Pirie A, Ramsell TG. Diabetes and the Eye. Oxford: Blackwell Scientific, 1969: chapter 6. 7. Owens DR, Vprlund A, Jones D, et a/. Retinopathy in newly presenting non-insulin dependent (Type 2) diabetic patients. Diabetes Res 1988; 9: 59-65. 8. Klein R, Klein BEK, Moss SE, et a/. The Wisconsin Epidemiological Study of Diabetic Retinopathy. I l l Prevalence and risk of diabetic retinopathy when age of diagnosis i s 30 or more years. Arch Ophthalmol 1984 102: 527-532. 9. Dwyer MS, Melton LJ, Ballard DJ, et a/. incidence of diabetic retinopathy and blindness: A population-based study in Rochester, Minnesota. Diabetes Care 1985; 8: 316-322. 10. Aiello LM, Rand LI, Briones JC, Wafai MZ, Sebestyen JG. Diabetic retinopathy in Joslin Clinic Patients with adultonset diabetes. Ophthalmology 1981; 88: 619-623. 11. The Diabetic Retinopathy Study Research Group. Photocoagulation treatment of pro1iferative diabetic retinopathy. Diabetic Retinopathy Study Report No. 8. Ophthalmology 1981; 88: 583-600. 12. British Multicentre Study Group. Photocoagulation for proliferative diabetic retinopathy: a randomised controlled clinical trial using the xenon-arc. Diabetologia 1984; 26: 109-1 15. 13. British Multicentre Study Group. Photocoagulation for diabetic maculopathy: a randomised controlled clinical trial using the xenon-arc. Diabetes 1984; 32: 1010-1 01 6. 14. The Early Treatment Diabetic Retinopathy Study Research Group. Photocoagulation for diabetic macular oedema. Early Treatment Diabetic Retinopathy Study Report No. 1. Arch Ophthalmol 1985; 103: 1796-1806. 15. Grey RHB, Burns-Cox CJ, Hughes A. Blind and partial sight registrations in Avon. Br J Ophthalmol 1989; 73: 88-94. 16. Aclimandos WA, Galloway NR. Blindness in the city of Nottingham (1980-85). €ye 1988; 2: 431-434. 17. Bresnick GH. Methods to quantify diabetic retinopathy: structural and functional. In: Andreani D, Crepaldi G, DiMario U, Pozza G, eds. Diabetic Complications: Early Diagnosis and Treatment. 1985; 8: 73-89. 18. Scott GI. Ocular complications of diabetes mellitus. Br J Ophthalmol 1953; 37: 705-71 5. 19. Oakley N, Hill DW, Joplin GF, Kohner EM, Fraser TR. Diabetic retinopathy. The assessment of severity and progress by comparison with a set of standard fundus photographs. Diabetologia 1967; 3: 402-405. 20. Davis MD, Norton EWD, Myers FL. Airlie classification of diabetic retinopathy. In: Goldbery MF, Fine SL, eds. Symposium on the Treatment of Diabetic Retinopathy. Washington DC:Public Health Service Publication No. 1890, 1968. 21. Klein BEK, Davis MD, Segal P, et a/. Diabetic retinopathy: assessment of severity and progression. Ophthalmology 1984; 91: 10-17. 22. Ferris FL, Kassoff A, Bresnick GH, et a/. New visual acuity charts for clinical research. Am / Ophthalmol 1982; 94: 91-96. 23. Bowman KJ. A method for quantitative scoring of the Farnsworth Panel D-15. Acta Ophthalmol 1982; 60: 907-91 6. SCREENING FOR DIABETIC RETINOPATHY
SYMPOSIUM PROCEEDINGS 24. 25. 26.
27.
28.
29. 30.
31. 32.
33. 34. 35. 36. 37.
38.
39.
40. 41.
42.
43.
Hyvarinen L, Laurinen P, Rovamo J. Contrast sensitivity in evaluation of visual impairment due to diabetes. Acta Ophthalmol 1983; 61 : 94-1 01. Bresnick GH. Diabetic retinopathy viewed as a neurosensory disorder. Arch Ophthalmol 1986; 104: 989-990. National Institute of Health, Office of Scientific Reporting. Diabetes and Your Eyes. Bethesda: Dept of Health and Human Sciences, 1983. (DHSS Publication No. (NIM) 83-21 71 :3.) Foulds WS, MacCuish AS, Barrie T, et a/. Diabetic retinopathy in the West of Scotland: its detection and prevalence and the cost-effectiveness of a proposed screening programme. Edinburgh: Health Bull 1983; 41 : 3 19-326. Moss SE, Klein R, Kessler SD, Richie KA. Comparison between ophthalmoscopy and fundus photography in determining severity of diabetic retinopathy. Ophthalmology 1985; 92: 62-67. Palmberg P, Smith M, Waltman S, et a/. The natural history of retinopathy in insulin dependent juvenile-onset diabetes. Ophthalmology 1981; 88: 613-61 8. The Diabetes Control and Complications Trial Research Group. Colour Photography vs Fluorescein angiography in the detection of diabetic retinopathy in the Diabetes Control and Complication Trial. Arch Ophthalmol 1987; 105: 1344-1 357. Sussman EJ, Tsiaras WG, Soper KA. Diagnosis of diabetic eye disease. IAMA 1982; 247: 3231-3234. Spathis GS. Facilities in diabetic clinics in the UK: shortcomings and recommendations. Medical Advisory Committee of the British Diabetic Association. Diabetic Med 1986; 3: 131-136. Editorial. Treatment of diabetic retinopathy. Lancet 1984; i: 439-440. Burns-Cox CJ, Dean-Hart JC. Screening of diabetics for retinopathy by ophthalmic opticians. Br M e d l 1985; 290: 1052-1 054. Forrest RD, JacksonCA, Yudkin IS. Screening for diabetic retinopathy-comparison of a nurse and a doctor with retinal photography. Diabetes Res 1987; 5 : 39-42. Ohri R, Kohner EM. Screening for diabetic retinopathy. The ocular examination of diabetic patients. Practical Diabetes 1986; 3: 214-215. Ryder REJ, Vora JP, Atiea JA, Owens DR, Hayes TM, Young S. Possible new method to improve detection of diabetic retinopathy: Polaroid non-mydriatic retinal photography. Br Med I 1985; 291 : 1256-1 257. Ryder REJ, Young S, Vora JP, Atiea JA, Owens DR, Hayes TM. Screening for diabetic retinopathy using Polaroid retinal photography through undilated pupils. Practical Diabetes 1985; 2: 34-40. Klein R, Klein BEK, Neider MW, Hubbard LD, Mener SM, Brothers RJ. Diabetic retinopathy as detected using ophthalmoscopy, a non mydriatic camera and a standard fundus camera. Ophthalmology 1985; 92: 485-491. Ryder REJ, Hayes TM. Non-mydriatic retinal photography in screening for diabetic retinopathy. Seminars in Ophthalmology 1987; 2: 26-29. Jones D, Dolben J, Owens DR, Vora JP, Young S, Creagh FM. Non-mydriatic Polaroid photography in screening for diabetic retinopathy: evaluation in a clinical setting. Br Med / 1988; 296: 1029-1030. Taylor R, Lovelock L, Tunbridge WMG, et a/. Comparison of non-mydriatic Polaroid photography with fundoscopy in 2159 patients: Final results of BDA Mobile Camera Study. Diabetic Med 1989; 6: (suppl 1): A23. Williams R, Nussey S, Humphry R, Thompson G. Assessment of non-mydriatic fundus photography in detection of diabetic retinopathy. Br Med / 1986; 293: 1140-1 142.
s9
DTT7
SYMPOSIUM PROCEEDINGS Barrie T, MacCuish AC. Assessment of non-mydriatic fundus photography in detection of diabetic retinopathy. Br Med I 1986; 293: 1304-1 305. 45. Rosen ES, Raines M, Hancock R. Use of non-mydriatic cameras to screen diabetic patients for retinopathy. Seminars in Ophthalmology 1987; 2: 37-44. 46. Dollery CT, Hodge JW, Engel M. Studies of the retinal circulation with fluorescein. Br Med 1962; 2: 1210-1 21 5. 47. Yassur Y, Axer-Siege1 R, Ben-Sira I. Early detection of diabetic retinopathy by fundus photography using 44.
s10
48. 49. 50.
monochrome light. In: Fin. Ovens (ed). Management of retinal vascular and macular disorders. Baltimore: Williams & Wilkins, 1983: 58-60. Kelly IS, Kincaid M, Hoover RE, McBeth C. Retinal fluorograms using oral fluorescein. Ophthalmology 1980; 85: 805-81 1. Azad R, Nayak BK, Tewar HK, Khosla PK. Oral fluorescein angiography. Indian I Ophthalmol 1984; 32: 415 4 1 7. The Oral Fluorescein Study Group. Oral fluorography. I Am Optometric Assoc 1985; 56: 784-792.
D.R. OWENS ET AL.
S Y M P O S I U M PROCEEDINGS
Screening for Diabetic Retinopathy D.R. Owens, J. Dolben, S. Young, R.E.J. Ryder, I.R. Jones, T.M. Hayes
J.Vora,
D. Jones, D. Morsman,
Diabetes Research Unit, Department of Medicine, University of Wales College of Medicine, Heath Park, Cardiff, UK
There is a need for greater educational emphasis, both at undergraduate and postgraduate level, on the detection of diabetic eye disease, in particular diabetic retinopathy. The early diagnosis of the sight-threatening lesions of proliferative retinopathy and maculopathy is a prerequisite for the prevention or reduction of the visual loss and blindness associated with this diabetic complication. It i s also essential that patients are aware that diabetes can result in visual loss due to diabetic retinopathy. Patients should understand that diabetic retinopathy may be present without ophthalmic or diabetic symptoms and that its incidence increases with duration of diabetes, poor diabetes control, and hypertension. They must also be aware that, if detected early, retinopathy can be treated successfully and vision preserved. Early detection depends on regular eye examination involving both visual acuity assessment and ophthalmoscopy through dilated pupils by experienced personnel. A comprehensive programme of screening followed by prompt and adequate treatment would made a significant contribution to eradicating diabetic retinopathy as a cause of blindness. KEY WORDS
Diabetic retinopathy Screening Clinical examination Fundus photography
Introduction
efficacy of local treatment with laser photocoagulation, for both proliferative retinopathy and maculopathy is now Long-standing diabetes mellitus results in significant well established and should preferably be instituted diabetic eye disease chiefly affecting the retina (diabetic before the onset of those retinal symptoms associated with retinopathy) and lens (cataract). Diabetic retinopathy is significant visual loss.' 1-14 Photocoagulation produces a a leading cause of blindness in adults between 25 and clear difference in the deterioration rate between treated 74 years of age.14 Up to 98 % of insulin-treated patients and untreated eyes in patients with proliferative retinopadiagnosed before the age of 30 years will have evidence thy. This is especially noticeable in eyes labelled high of diabetic retinopathy after 20 years of diabetes. Sightrisk in whom 50 % of controls and only 15 % of treated threatening proliferative retinopathy may be present in eyes became blind over a 5-year period.",'* In eyes with 50 % of these patients increasing to 67 % after 35 years.5 mild-to-moderate non-proliferative diabetic retinopathy In contrast, up to 20 % of non-insulin-treated patients and macular oedema, deterioration after 3 years occurred have some diabetic retinopathy even at diagn~sis,~,' in 24 % of untreated eyes compared to 12 % of treated increasing to approximately 50 % after a duration of 20 eyes. 3,1 years or more.c1o For the same period of time the Despite these important advances and in view of the prevalence of proliferative retinopathy increases from increasing size of the diabetic population, little or Although the incidence rate of around 5 to 20 no reduction in the overall incidence of new blind retinopathy is two- or three-fold greater amongst Type 1 registrations due to diabetes has yet been achieved.15,16 (insulin-dependent)than Type 2 (non-insulin-dependent) Therefore, the justification and need for retinopathy diabetic patients, the latter is a much larger group and screening in diabetic patients is overwhelming, because contributes over four times more retinopathies. Type 2 it is common, often asymptomatic, and yet eminently diabetic patients represent the major proportion of treatable (especially if detected early). Noteworthy is the diabetic patients requiring ophthalmological care.'O impressive reduction in the rate of blind registration due Proliferative retinopathy is the major occular problem to glaucoma and cataract during the last 20 years which faced by the Type 1 diabetic patient, with maculopathy has been as a direct result of improved medical and the most important for the Type 2 diabetic ~ a t i e n t . ~ , ~ , surgical techniques.' 5 , 1 6 *lo Whereas diabetic retinopathy is rarely a threat to The ability to detect, classify, and quantify diabetic vision during the first 10 years for the Type 1 diabetic retinopathy in a reliable way is necessary if an appropriate patient, this is certainly not the case for the Type 2 management programme is to be chosen for individual diabetic patient with an unknown duration of disease. The patient^.'^ Methods adopted can be divided into those aimed at detecting morphological changes and those which detect functional abnormalities. For morphological changes, considerable advances have been achieved Correspondence to: Dr D.R. Owens, Diabetes Research Unit, Departover the last 20 to 30 years using fundus photography ment of Medicine, University of Wales College of Medicine, Heath Park, Cardiff, UK. in an attempt to classify diabetic retinopathy and grade s4
0742-3071/91/Symposium 0004-07$05.00 & Sons, Ltd.
0 1991 by John Wiley
DIABETIC MEDICINE, 1991; 8 Symposium: S4-S10
nm its severity according to structural The structural abnormalities associated with diabetic retinopathy are usually classified as non-proliferative or proliferative. Non-proliferative diabetic retinopathy refers to intraretinal abnormalities including: microaneurysms, dilated retinal capillaries, retinal haemorrhages, cotton wool spots (ischaemic infarcts), hard exudates, and retinal oedema. These changes can be understood in terms of two underlying and basic pathophysiological processes: retinal vessel closure and abnormal retinal vessel permeability. Proliferative diabetic retinopathy consists of proliferation of fibrovascular and glial tissue in front of the retina; a process thought to be a response to underlying retinal ischaemia. New, (pre-retinal) vessels, at the disc or elsewhere, can cause pre-retinal and vitreous haemorrhage. Vitreous and retinal detachment may result from the shrinkage of the fibrous and glial tissue. Functional abnormalities associated with diabetic retinopathy such as visual acuity, colour vision, perimetry, and contrast sensitivity also lend themselves to q ~ a n t i f i c a t i o n . ~The ~ - ~ presence ~ of functional abnormalities of the retina, and therefore visual disability, may not only indicate the extent of diabetic retinopathy but may precede clinically visible retinopathy and even predict future events. Currently, 1 to 2 % of all diabetic patients are blind or partially sighted14 with between 50 and 70 % of blindness from both proliferative retinopathy and maculopathy being preventable by early detection and treatrnent."-I4 A much larger proportion of patients not registered as blind, but greatly handicapped by visual loss,26 would benefit from an improved level of ophthalmological care. Therefore, it is mandatory to establish an effective screening programme for diabetic eye disease in an attempt to prevent or limit visual loss and blindness from diabetic retinopathy.
SYMPOSIUM PROCEEDINGS conditions which prevail in the majority of busy hospital diabetic and general practitioner clinics, potentially serious misdiagnosis may easily occur and treatable lesions go ~ n d e t e c t e d .It~ has ~ been estimated that up to 10 % of the population attending a diabetic clinic has serious retinopathy, many of whom remain undetected and therefore untreated.33Alternative screening methods therefore need to be considered. At primary care level, screening by ophthalmic opticians in Great Britain confirms their ability to accurately detect abnormalities of the fundus in diabetic patients.34 Their involvement in screening has proved successful in many centres and could be more widely adopted. Evidence from several studies indicates that adequate training is an essential prerequisite for both medical and non-medical personnel involved in detecting diabetic r e t i n ~ p a t h y . ~ ~
Clinical Examination
The first essential step in any screening programme i s to take a detailed history from the patient with special reference to the duration of diabetes and to visual ~ y m p t o m s . As ~ ~ retinopathy may deteriorate during pregnancy, all women with diabetes should, where possible, be examined before the commencement of pregnancy and at 3-monthly intervals throughout the pregnancy. Diabetic patients with hypertension, renal disease or prolonged poor glycaemic control (necessitatinga change in therapy) must also be regarded as at high risk. The assessment of visual acuity remains the mainstay for measuring central retinal and higher order visual function. It is generally carried out using standardized Snellen visual acuity charts, adequately illuminated at a defined distance. One eye is tested at a time and the refractive error corrected if the visual acuity is worse than 6/6 using the patient's spectacles for distance vision. The use of a pinhole card can overcome refractive errors Screening for Diabetic Retinopathy but cannot improve vision. The 'pinhole test' can assist in the differentiation between impaired vision due to The onus to detect and institute treatment for diabetic either refractive error or pathology in the eye. General retinopathy rests with both physician and ophthalmoleye examination follows for the presence of cataract ogist. In any programme of screening it is essential to formation and evidence of rubeosis. The patient is then establish how and when to screen and who should be prepared for fundal examination using a short-acting involved at each stage. Improved education for the mydriatic such as tropicamide (0.5 to 1 %) or phenylephprofessional, patients, and the public is therefore required. rine (2.5 to 10 %). Mydriasis carries a small risk of Ophthalmoscopy by an ophthalmologist aided by precipitating acute glaucoma. Patients known to have fluorescein angiography and colour photography of the glaucoma or having a previous history of eye surgery are fundus affords the most sensitive and specific means best assessed by an ophthalmologist. An efficient working of detecting and assessing diabetic r e t i n ~ p a t h y . ~ ~ ,ophthalmoscope ~~ is a prerequisite for adequate ophthalStereophotography and angiography are both superior to moscopy. ophthalmos~opy with ~ ~ the ~~~ two techniques essentially In diabetic patients diagnosed before the age of 30 of comparable accuracy.3o Under optimal conditions, years, the first retinal examination should occur no later approximately 30 % of physicians with an interest in than 5 years after diagnosis with annual checks from 10 diabetes may fail to diagnose proliferative diabetic years onwards. For patients diagnosed after 30 years of retinopathy by ophthalm~scopy.~'The failure rate can age, retinae should be checked at diagnosis with a increase to an alarming 50 % in the case of more follow-up examination every year. More frequent review junior medical ~ t a f f . ~Therefore, ' under the suboptimal is recommended once lesions of diabetic retinopathy
SCREENING FOR DIABETIC RETINOPATHY
s5
SYMPOSIUM PROCEEDINGS
Dm
are observed. Additional checks are required during pregnancy, and in high-risk patients.
As sight-threatening lesions of diabetic retinopathy may not be detected from Polaroid colour prints obtained with non-mydriatic fundal cameras we conducted a study to compare Polaroid prints in a 'field' situation with Retinal Photography 35 mm colour transparencies (with mydriasis) and fluorIn an attempt to produce a screening procedure that escein angi~grams.~'Eighty-three per cent (105/127) of does not require ophthalmological expertise, various the Polaroid prints were considered assessable compared photographic techniques have been developed. It has to 98 % (124/127) of colour transparencies and 98 % clearly been demonstrated that stereoscopic fundal photo(125/127) of fluorescein angiograms (Table 1). The pickgraphs are more accurate than simple ophthalmoscopic up rate of microaneurysms, haemorrhages, hard exudates, examination,28 with the combination of fluorescein and cotton wool spots was essentially similar for the angiography and colour photographs representing the Polaroid prints and 35 mm transparencies of equivalent most accurate description of retinal m o r p h ~ l o g y . ~ ~ quality (Table 2). Fluorescein angiography revealed a 5 to 8 times greater number of microaneurysms and was Recently the introduction of non-mydriatic 45" cameras superior in detecting new vessels, cotton wool spots, has offered the possibility of large-scale screening without the need for m y d r i a ~ i s . ~The ' ~ ~ Canon CR2-45NM and macular oedema although difficulty in detecting exudative and haemorrhagic lesions was experienced. In (Clement Clark Ltd, London, UK) and Topcon TRC NWtwo cases early disc new vessels were not seen on 2 (Keeler Ltd, London, UK) require a minimal pupil Polaroid prints. The overall detection rate of diabetic diameter of 5 mm and the Canon CR3-NM and Kowa Nonmyd plus (Keeler Ltd, London, UK) cameras a retinopathy in this patient population was 74 % and minimal diameter of 4 mm. Canon CR3-45NM has a 88 % for Polaroid prints and 35 mm transparencies, higher detection rate for diabetic r e t i n ~ p a t h y .The ~~ respectively (Table 3). However, both had limited camera shown in Figure 1 utilizes an infra-red television capacity to demonstrate the presence of preproliferative camera with a suitable filtered light source for viewing and proliferative diabetic retinopathy. the retina as a black and white retinal image on a A more recent study comparing non-mydriatic Polaroid television monitor, while the patient's eye is dark adapted. photography with fundoscopy in 2159 patients rePolaroid colour prints or transparencies obtained using emphasized the potential unreliability of both techniques the Kowa Nonmyd plus and CR3-45NM cameras can be when they are not carried out Under accurate and sensitive for detecting diabetic retinopathy controlled conditions non-mydriatic Polaroid photograin 96.5 % of cases.43Neverthelessan important limitation phy was deemed as good as routine clinic ophthalof the non-mydriatic camera is the restriction to a 45" moscopy through dilated pupils by non-ophthalmologists field, encompassing the disc-macula area. As 8 to 15 % and considerably more reliable for detecting maculopathy of all lesions of diabetic retinopathy and 27 % of cases at a treatable stage. of proliferative diabetic retinopathy reside outside the The rate of usable photographs (10 % were of poor 45" field, the technique is obviously r e ~ t r i c t e d . * ~ , ~ ~quality) ,~~ has been regarded by others to be too low when Although the use of a Polaroid camera makes fundal screening for the sight-threatening lesions of diabetic photographs available with little delay, the resolution of re ti no path^.^^ The potential role of the non-mydriatic camera has to be considered relative to the existing Polaroid film is frequently inadequate to record the presence of small, fine, new vessels with potentially methods of screening available in a variety of different serious consequence^.^!,^^ clinical situations. Its use can be advantageous where the medical staff are either inexperienced or insufficient to deal with the large number of diabetic patients. The camera is potentially useful when used by a trained operator and the prints read by an experienced observer. The observer must be fully aware of the limitations of the procedure and therefore able to decide either to rephotograph with or without mydriasis or refer the patient to an ophthalmologist. The camera is easy to use and provides a reasonably reliable photographic representation of the severity of retinopathy (in broad categories) within its 45" field of vision.39 It is superior to ophthalmoscopy through undilated pupils but cannot be relied upon to detect certain vision-threatening lesions such as macular oedema and early new vessel formation. The potential educational role of non-mydriatic Polaroid retinal photography should not be underestimated when used in parallel with ophthalmoscopy following mydFigure 1. The Canon CR3-4NM non-mydriatic retinal camera riasis. The photographs should assist with and emphasize S6
D.R. OWENS €7 AL.
Dm
SYMPOSIUM PROCEEDINGS Table 1. Quality grading of retinal photographs Quality grade”
Polaroid prints 35 rnrn Transparencies
1
2
3
4
5
60 (47) 116 (91)
45 (35) 8 (6)
18 (14) 2 (2)
4 (3) 1 (1)
0 (0) 0 (0)
Number (%). ’1 = Excellent clarity, 2 = definition of most retinal detail, 3 = limited definition, 4 = gross detail only visible, and 5 = no detail visible.
Table 2. Detection of retinal lesions by three photographic techniques based on assessable photographic records in eyes with diabetic retinopathy (n = 43) Polaroid prints Microaneurysrns Haemorrhages Hard exudates Macular oedema Cotton wool spots IRMA
New vessels
35 rnrn Fluorescein Transparencies angiograrns
5 28 27 2 4 1 0
9 33 26 2 5 0 1
38 19 8 5 12 1 2
IRMA: intraretinal microvascular abnormalities.
the virtues of direct ophthalmoscopy with mydriasis which should eventually make the non-mydriatic camera superfluous to requirements in the context of retinopathy screening. The non-mydriatic camera will not replace proper ophthalmoscopic examination by an experienced attending physician.
Oral fluorescein Fluorescein fundus angiography allows detailed examination of the retinal microcirculation (capillary bed) and retinal blood The presence of cystoid macular oedema, small tufts of new vessels, and leakage from such early neovascularization are clearly demonstrated.
Small haemorrhages and hard exudates may however be less obvious than on a colour p h ~ t o g r a p hThe . ~ ~ use of different filters for colour photography prior to dye injection enables identification and differentiation between exudates, haemorrhages, and retinal pigment defects. The technique of intravenous fluorescein angiography to detect early diabetic retinopathy is at present unsurpassed. However it must be appreciated that this method is associated with unwanted effects in a small proportion of patients. In our recent experience of 100 consecutive Type 2 diabetic patients, 81 had no sideeffects, 15 experienced mild nausea, vomiting occurred in 1, breathlessnesskoughing in 1, and 2 patients had a transient skin rash. This technique is therefore a relatively safe procedure provided the necessary precautions are observed. Orally administered fluorescein has been used by several investigators to circumvent a number of problems associated with the intravenous The procedure is deemed safer and simpler to perform, with better patient acceptance and provides documentation of late dye leakage (Figure 2). Colour photographs are taken between 30 and 60 min following the oral administration of sodium fluorescein in a sweetened drink. In some centres up to 10 % of fluorescein studies are done utilizing the oral which is especially useful in children, patients with difficult veins, and where repeated studies are necessary. The detection and assessment of responses to treatment of retinal vascular leakage especially macular oedema is an obvious area for expansion. It may also be used as an adjunct to Polaroid
Table 3. Comparison of detection rate according to type of retinopathy Diabetic retinopathy
Polaroid prints 35 rnrn Transparency Fluorescein angiogram
All patients
Background
Macular oederna
Preproliferative
Pro1iferative
32 (75) 38 (88) 43 (100)
25 30 26
2 2 3
5 5 12
0 1 2
Number (%). SCREENING FOR DIABETIC RETINOPATHY
s7
Dm
S Y M P O S I U M PROCEEDINGS
Figure 2. Oral fluorescein fundal angiography demonstrating late dye leakage
colour photography of the fundus with non-mydriatic cameras, thereby avoiding failure to detect sight-threatening lesions of cystoid macular oedema and proliferative diabetic retinopathy within a 45" field. Further work is still needed to determine the optimal procedure for this technique.
Conclusions Direct ophthalmoscopy by an experienced observer remains the best method of screening for the presence of diabetic retinopathy. Ophthalmoscopy by non-retinal specialists, through undilated pupils, is an insensitive and non-specific means of detecting or classifying diabetic retinopathy. Clearly there is an urgent need for more education of clinicians in the detection of diabetic eye disease, in particular diabetic retinopathy. The early diagnosis of the sight-threatening lesions of proliferative retinopathy and maculopathy is a prerequisite for the prevention or reduction of the visual loss and blindness associated with diabetic retinopathy. It is also necessary that the patient and the public are made aware that diabetes can result in visual loss. Patient education programmes should encourage an understanding that diabetic retinopathy may be present without ophthalmological symptoms. Patients should also be informed that duration of diabetes, poor diabetes control, and hypertension are associated with a higher incidence of diabetic retinopathy. Pregnancy i s also a time for vigilance. Patients must be aware that retinopathy can be treated successfully and vision preserved provided it is detected early enough. This means regular eye examination involving both visual acuity assessment and
S8
ophthalmoscopy through dilated pupils by experienced personnel. Non-mydriatic cameras have a place in screening for diabetic retinopathy especially where ophthalmological support is limited. Trained operators and experienced readers of the Polaroid prints are essential to avoid failure to diagnose treatable visionthreatening lesions. The cost benefit of the non-mydriatic cameras has to be assessed for each individual situation where diabetic retinopathy screening is considered. The use of oral fluorescein angiography in such screening programmes needs further evaluation. Considerable effort is necessary to initiate and maintain a comprehensive programme of screening for diabetic retinopathy to ensure timely intervention in an attempt to eliminate diabetic retinopathy as a cause of visual loss and blindness in diabetic patients.
Acknowledgements We wish to thank Debra Thomas for typing the manuscript and the Department of Medical Illustration, University Hospital of Wales, for the illustrations.
References Sorsby A. The Incidence and Causes of Blindness in Englandand Wales 1948-1962. Reports on Public Health and Medical Subjects No. 114. London: HMSO, 1966. 2 . Sorsby A. The Incidence and Causes of Blindness in England and Wales 1963-1968. Reports on Public Health and Medical Subjects No. 128. London: HMSO, 1972. 3. Kahn HA, Hiller R. Blindness caused by diabetic retinopa1.
D.R.OWENS E l
AL.
Dm thy. Am J Ophthalmol 1974; 78: 58-67. 4. Ghafour IM, Allen D, Foulds WS. Common causes of blindness and visual handicap in the West of Scotland. Br 1 Ophthalmol 1983; 67: 209-21 3. 5. Klein R, Klein BEK, Moss SE, et al. The Wisconsin Epidemiological Study of Diabetic Retinopathy. I1 Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol 1984; 102: 520-532. 6. Caird FL, Pirie A, Ramsell TG. Diabetes and the Eye. Oxford: Blackwell Scientific, 1969: chapter 6. 7. Owens DR, Vprlund A, Jones D, et a/. Retinopathy in newly presenting non-insulin dependent (Type 2) diabetic patients. Diabetes Res 1988; 9: 59-65. 8. Klein R, Klein BEK, Moss SE, et a/. The Wisconsin Epidemiological Study of Diabetic Retinopathy. I l l Prevalence and risk of diabetic retinopathy when age of diagnosis i s 30 or more years. Arch Ophthalmol 1984 102: 527-532. 9. Dwyer MS, Melton LJ, Ballard DJ, et a/. incidence of diabetic retinopathy and blindness: A population-based study in Rochester, Minnesota. Diabetes Care 1985; 8: 316-322. 10. Aiello LM, Rand LI, Briones JC, Wafai MZ, Sebestyen JG. Diabetic retinopathy in Joslin Clinic Patients with adultonset diabetes. Ophthalmology 1981; 88: 619-623. 11. The Diabetic Retinopathy Study Research Group. Photocoagulation treatment of pro1iferative diabetic retinopathy. Diabetic Retinopathy Study Report No. 8. Ophthalmology 1981; 88: 583-600. 12. British Multicentre Study Group. Photocoagulation for proliferative diabetic retinopathy: a randomised controlled clinical trial using the xenon-arc. Diabetologia 1984; 26: 109-1 15. 13. British Multicentre Study Group. Photocoagulation for diabetic maculopathy: a randomised controlled clinical trial using the xenon-arc. Diabetes 1984; 32: 1010-1 01 6. 14. The Early Treatment Diabetic Retinopathy Study Research Group. Photocoagulation for diabetic macular oedema. Early Treatment Diabetic Retinopathy Study Report No. 1. Arch Ophthalmol 1985; 103: 1796-1806. 15. Grey RHB, Burns-Cox CJ, Hughes A. Blind and partial sight registrations in Avon. Br J Ophthalmol 1989; 73: 88-94. 16. Aclimandos WA, Galloway NR. Blindness in the city of Nottingham (1980-85). €ye 1988; 2: 431-434. 17. Bresnick GH. Methods to quantify diabetic retinopathy: structural and functional. In: Andreani D, Crepaldi G, DiMario U, Pozza G, eds. Diabetic Complications: Early Diagnosis and Treatment. 1985; 8: 73-89. 18. Scott GI. Ocular complications of diabetes mellitus. Br J Ophthalmol 1953; 37: 705-71 5. 19. Oakley N, Hill DW, Joplin GF, Kohner EM, Fraser TR. Diabetic retinopathy. The assessment of severity and progress by comparison with a set of standard fundus photographs. Diabetologia 1967; 3: 402-405. 20. Davis MD, Norton EWD, Myers FL. Airlie classification of diabetic retinopathy. In: Goldbery MF, Fine SL, eds. Symposium on the Treatment of Diabetic Retinopathy. Washington DC:Public Health Service Publication No. 1890, 1968. 21. Klein BEK, Davis MD, Segal P, et a/. Diabetic retinopathy: assessment of severity and progression. Ophthalmology 1984; 91: 10-17. 22. Ferris FL, Kassoff A, Bresnick GH, et a/. New visual acuity charts for clinical research. Am / Ophthalmol 1982; 94: 91-96. 23. Bowman KJ. A method for quantitative scoring of the Farnsworth Panel D-15. Acta Ophthalmol 1982; 60: 907-91 6. SCREENING FOR DIABETIC RETINOPATHY
SYMPOSIUM PROCEEDINGS 24. 25. 26.
27.
28.
29. 30.
31. 32.
33. 34. 35. 36. 37.
38.
39.
40. 41.
42.
43.
Hyvarinen L, Laurinen P, Rovamo J. Contrast sensitivity in evaluation of visual impairment due to diabetes. Acta Ophthalmol 1983; 61 : 94-1 01. Bresnick GH. Diabetic retinopathy viewed as a neurosensory disorder. Arch Ophthalmol 1986; 104: 989-990. National Institute of Health, Office of Scientific Reporting. Diabetes and Your Eyes. Bethesda: Dept of Health and Human Sciences, 1983. (DHSS Publication No. (NIM) 83-21 71 :3.) Foulds WS, MacCuish AS, Barrie T, et a/. Diabetic retinopathy in the West of Scotland: its detection and prevalence and the cost-effectiveness of a proposed screening programme. Edinburgh: Health Bull 1983; 41 : 3 19-326. Moss SE, Klein R, Kessler SD, Richie KA. Comparison between ophthalmoscopy and fundus photography in determining severity of diabetic retinopathy. Ophthalmology 1985; 92: 62-67. Palmberg P, Smith M, Waltman S, et a/. The natural history of retinopathy in insulin dependent juvenile-onset diabetes. Ophthalmology 1981; 88: 613-61 8. The Diabetes Control and Complications Trial Research Group. Colour Photography vs Fluorescein angiography in the detection of diabetic retinopathy in the Diabetes Control and Complication Trial. Arch Ophthalmol 1987; 105: 1344-1 357. Sussman EJ, Tsiaras WG, Soper KA. Diagnosis of diabetic eye disease. IAMA 1982; 247: 3231-3234. Spathis GS. Facilities in diabetic clinics in the UK: shortcomings and recommendations. Medical Advisory Committee of the British Diabetic Association. Diabetic Med 1986; 3: 131-136. Editorial. Treatment of diabetic retinopathy. Lancet 1984; i: 439-440. Burns-Cox CJ, Dean-Hart JC. Screening of diabetics for retinopathy by ophthalmic opticians. Br M e d l 1985; 290: 1052-1 054. Forrest RD, JacksonCA, Yudkin IS. Screening for diabetic retinopathy-comparison of a nurse and a doctor with retinal photography. Diabetes Res 1987; 5 : 39-42. Ohri R, Kohner EM. Screening for diabetic retinopathy. The ocular examination of diabetic patients. Practical Diabetes 1986; 3: 214-215. Ryder REJ, Vora JP, Atiea JA, Owens DR, Hayes TM, Young S. Possible new method to improve detection of diabetic retinopathy: Polaroid non-mydriatic retinal photography. Br Med I 1985; 291 : 1256-1 257. Ryder REJ, Young S, Vora JP, Atiea JA, Owens DR, Hayes TM. Screening for diabetic retinopathy using Polaroid retinal photography through undilated pupils. Practical Diabetes 1985; 2: 34-40. Klein R, Klein BEK, Neider MW, Hubbard LD, Mener SM, Brothers RJ. Diabetic retinopathy as detected using ophthalmoscopy, a non mydriatic camera and a standard fundus camera. Ophthalmology 1985; 92: 485-491. Ryder REJ, Hayes TM. Non-mydriatic retinal photography in screening for diabetic retinopathy. Seminars in Ophthalmology 1987; 2: 26-29. Jones D, Dolben J, Owens DR, Vora JP, Young S, Creagh FM. Non-mydriatic Polaroid photography in screening for diabetic retinopathy: evaluation in a clinical setting. Br Med / 1988; 296: 1029-1030. Taylor R, Lovelock L, Tunbridge WMG, et a/. Comparison of non-mydriatic Polaroid photography with fundoscopy in 2159 patients: Final results of BDA Mobile Camera Study. Diabetic Med 1989; 6: (suppl 1): A23. Williams R, Nussey S, Humphry R, Thompson G. Assessment of non-mydriatic fundus photography in detection of diabetic retinopathy. Br Med / 1986; 293: 1140-1 142.
s9
DTT7
SYMPOSIUM PROCEEDINGS Barrie T, MacCuish AC. Assessment of non-mydriatic fundus photography in detection of diabetic retinopathy. Br Med I 1986; 293: 1304-1 305. 45. Rosen ES, Raines M, Hancock R. Use of non-mydriatic cameras to screen diabetic patients for retinopathy. Seminars in Ophthalmology 1987; 2: 37-44. 46. Dollery CT, Hodge JW, Engel M. Studies of the retinal circulation with fluorescein. Br Med 1962; 2: 1210-1 21 5. 47. Yassur Y, Axer-Siege1 R, Ben-Sira I. Early detection of diabetic retinopathy by fundus photography using 44.
s10
48. 49. 50.
monochrome light. In: Fin. Ovens (ed). Management of retinal vascular and macular disorders. Baltimore: Williams & Wilkins, 1983: 58-60. Kelly IS, Kincaid M, Hoover RE, McBeth C. Retinal fluorograms using oral fluorescein. Ophthalmology 1980; 85: 805-81 1. Azad R, Nayak BK, Tewar HK, Khosla PK. Oral fluorescein angiography. Indian I Ophthalmol 1984; 32: 415 4 1 7. The Oral Fluorescein Study Group. Oral fluorography. I Am Optometric Assoc 1985; 56: 784-792.
D.R. OWENS ET AL.
