] Diab Comp, 6:247-253
Nonmydriatic Fundus Photography in Screening for Treatable Diabetic Retinopathy ]ennifer B. Marks
ABSTRACT Diabetic retinopathy is a complication of both insulin-dependent (type I1 and non-insulindependent (type II) diabetes. The American Diabetes Association and others recommend screening for retinopathy, beginning 5 years after onset of symptoms for patients with type I diabetes and at the time of diagnosis for patients with type II diabetes. Ideally, diabetic patients are evaluated at recommended intervals by an ophthalmologist. Realistically, however, this is often not feasable, for reasons both of cost and availability. There is evidence that many diabetic patients are being referred too late for intervention, perhaps in part due to lax screening and detection, often the responsibility of internists and other primary care physicians. Data supports
the need for a cheap, widely available, easy-to-use, effective screening tool for detecting treatable diabetic retinopathy. To this end, several studies have evaluated nonmydriatic fundus photography, and compared it with more-established methods of detecting diabetic retinal disease. The real question to be considered is whether nonmydriatic fundus photography will help to detect early treatable retinopathy better than the average physician using ophthalmoscopy. Several studies support its usefulness in this regard, and are discussed in this review. Questions remain, however, and further study is warranted in evaluating its potential role. (Journal of Diabetes and Its Complications, 6;4:247-253, 1992.1
INTRODUCTION
or advanced proliferative retinopathy. It is of importance that many patients at high risk for visual loss are asymptomatic. Therefore, the American Diabetes Association and other&* recommend screening for retinopathy, beginning 5 years after onset of symptoms for patients with type I diabetes and at the time of diagnosis for patients with type II diabetes. Screening strategies and recommendations are based on the fact that, in general, the development and progression of diabetic retinopathy is orderly, advancing from mild background abnormalities through a preproliferative to a proliferative stage, each characterized by retinal changes which can be recognized and, when appropriate, treated. The results of several different randomized trials3f4 have clearly established the efficacy of laser treatment in preserving vision in diabetic patients with proliferative retinopathy and macular edema and more than justify screening for this complication.
iabetic retinopathy is a complication of both insulin-dependent (type I) and non-insulin-dependent (type II) diabetes. By 20 years duration of disease, nearly all type I and more than 60% of type II diabetic patients have some degree of retinopathy. Despite the availability of effective treatment, it remains the leading cause of blindness in working-age adults in industrialized countries. Visual loss results from either maculopathy
D
From the Department of Medicine, Division of Endocrinology, University of Miami School of Medicine, Miami, Florida, USA. Reprint requests to be sent to: Dr. Jennifer B. Marks, Department of Medicine, Division of Endocrinology, University of Miami School of Medicine, 1500 NW 12 Avenue, Jackson Medical Towers, Miami, FL 33136. 0 1992 ]ournal of Diabetes and Its Complications
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In the ideal world, diabetic patients are evaluated at recommended intervals by an ophthalmologist. Realistically, however, this is often not feasable, for reasons of both cost and availability. Office examinations of this nature are often not covered by Medicare or private insurance carriers. Moreover, it has been estimated that 8% of patients with diabetes mellitus in the United States have no health insurance.5 Screening is therefore left to physicians who may or may not understand the importance of detecting treatable retinopathy, possess the skill to identify significant retinopathy by direct ophthalmoscopic exam, or be aware of the indications for referral for treatment.6,7 Indeed, diabetologists and general internists have been shown to misdiagnose serious retinal lesions when performing direct ophthalmoscopy through a dilated pupil’ although with motivation, this skill can be imtraining, and experience, proved.9,*0 Data suggest that many primary care physicians do not even include ophthalmoscopy as part of the routine examination of their diabetic patients,9,11,12 and even less frequentIy utilize mydriasis9,12 Moreover, there is evidence that many diabetic patients are being referred too late for intervention,
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perhaps in part due to lax screening and detection.13-*5 There exists, therefore, a need for a cheaper, widely available, easy-to-use, effective screening tool for detecting treatable diabetic retinopathy. To this end, several studies have evaluated nonmydriatic fundus photography, and compared it with more-established methods of detecting diabetic retinal disease. Despite ongoing controversy regarding its effectiveness in identifying high-risk lesions, its clinical use is increasing, and it is being advocated a a method for screening for diabetic retinopathy.16,17 USE OF THE NONMYDRIATIC FUNDUS CAMERA The nonmydriatic fundus camera provides an instant color photograph, on Polaroid film, of a 45-degree field of the retina, including the macula and the optic disc, through an undilated pupil (Figure 1). The first eye is photographed after approximately 5 min of adaptation in a darkened room; the second, 5-10 min later, to allow the pupils time to dilate after the first flash. Data suggest that the procedure is well tolerated by patients,l’,‘* and the camera is relatively easy to use.l*
FIGURE 1 Polaroid photograph of a 45-degree field of a normal retina ~ taken with the Canon nonmydriatic ’ fundus camera, showing the macula and the optic disc.
] Diab Comp 1992; 6:4
Technical problems, however, are not infrequently encountered. Difficulty in obtaining photographs of good quality may occur as a result of many factors. Camera failure, i.e., failure of flash, was responsible for loss of approximately 30% of photographs in one study. I8 Lens opacities or cataracts, and inadequate pupillary mydriasis occur to a variable degree, particularly in more elderly populations with long duration of disease.1s,19 Artifacts and inexact focusing are other problems that may result in unsatisfactory photographs. I8 In studies evaluating the quality of photographs, the percentage of those that are unusable varies, and may range from as low as 4%-6%17,20,21 to as high as 22% -25%. 22,23This percentage may be somewhat lower if photographs are taken through a pharmacologically dilated pupil. *8,24,25 Several studies have compared the accuracy of nonmydriatic photography with various other methods to detect diabetic retinopathy, including direct and indirect ophthalmoscopy through both undilated and pharmacologically dilated pupils, stereoscopic photography, and fluorescein angiography. EFFICACY OF THE NONMYDRIATIC CAMERA FOR DETECTING SIGNIFICANT RETINOPATHY-COMPARISONS WITH OPHTHALMOSCOPY A study from the University Hospital of Wales23 evaluated the ability of physicians in a busy diabetic clinic to identify retinopathy by direct ophthalmoscopic examination through both dilated and undilated pupils, compared with detection of retinopathy by photographs taken with the nonmydriatic fundus camera. Of 137 eyes studied, the physicians found 24 with diabetic retinopathy present by photograph, whereas only 2 of those eyes had been identified by examination through undilated pupils, and only 8 through dilated pupils. In a repeat trial, the physicians achieved marginally better results. Of 90 eyes studied, 21 showed diabetic retinopathy on the photographs, whereas only 9 of those were detected by ophthalmoscopy through undilated pupils and only 8 through dilated pupils. That is, the photographs identified 23% of eyes as having some degree of retinopathy, while direct examination through undilated and dilated pupils identified 10% and 13%, respectively; a striking difference in detection rate. The authors concluded from this data that nonmydriatic fundus photography is an effective means of increasing the rate of identification of diabetic retinopathy in a busy diabetic clinic where ophthalmoscopy is overlooked or performed in a hurried manner. Other studies in similar clinical settings have found similar results,11,22,26but unfortunately provide no information regarding the actual efficacy of the technique in question, only showing it to be superior when compared with subop-
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timal ophthalmologic exams. In certain situations, of course, this may be important. In Britain, the Health Economics Research Group2’ evaluated 6304 eyes of 3318 diabetic patients in three general diabetic clinics using nonmydriatic fundus photography. Photographs were taken by specially trained ophthalmologic assistants and evaluated by hospital-based physicians and community general practitioners. Their diagnoses compared favorably to the diagnoses made by ophthalmologic exam performed by ophthalmologic opticians through dilated pupils. The sensitivities of all three techniques for detecting either proliferative retinopathy or maculopathy, however, were low (67% and 53% for photographs versus 47% for exams), despite a large proportion of fair-to-excellent quality photos (76%). These globally poor rates of detection are more likely a reflection of the lack of knowledge, experience, and/ or skills of the examiners, rather than the efficacy of nonmydriatic fundus photography, to detect retinopathy. The authors readily admit the lack of a ‘gold standard’ in this study, with exams performed by opticians being the reference standard for comparison to photographic results. Researchers at St. George’s Hospital in London*l also compared nonmydriatic fundus photography to ophthalmoscopy, but an experienced ophthalmologist performed the direct and indirect examinations through dilated pupils, a higher standard for comparison than that of either of the previous two studies. The photographs were also interpreted by more qualified readers, two ophthalmologists who were masked to the results of their colleague’s examinations. The results showed that the percentage of eyes identified as having three broad categories of retinopathy on the photographs compared favorably with the ophthalmologist’s diagnoses by examination: any retinopathy (58% versus 60%, respectively), maculopathy (27% for each), and neovascularization (7.5% versus 6.7%). Ophthalmoscopy identified retinopathy in 71 of 120 eyes; this was detected by the camera with an overall sensitivity of 96%, a specificity of 98%, a false negative rate of 6.8%, and false positive rate of 2%. The sensitivities and specificities for detecting maculopathy (n = 32) and neovascularization (n = 11) were 100% and 96%, and 82% and lOO%,respectively. Using this data and an approximate prevalence of retinopathy in a general diabetic clinic of lo%, the positive and negative predictive values are calculated to be 84% and 99.5%, respectively. That is, if retinopathy was identified on the photographs, it was 84% likely to be correct, whereas if retinopathy was not identified, it was 99.5% likely to be correct. In essence, then, based on these data, nonmydriatic fundus photography should detect most retinopathy, and, with such high specificity, would falsely identify few normal eyes as having
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retinopathy, thus wasting little money on unnecessary referrals for further evaluation or intervention. The authors’ conclusion, that nonmydriatic fundus photography, with later interpretation of photographs by an ophthalmologist, is an effective screening method for detection of diabetic retinopathy, would appear valid. The results of this study, however, have been criticized as being at variance with the experience of others. I9 A reasonable concern is that photographs taken with the nonmydriatic fundus camera miss important retinal lesions, particularly in the peripheral retina, which the camera does not photograph, or in the eyes of patients with small pupils or lens opacities. As not all clinical settings will have an opthalmologist available for interpretation of nonmydriatic photographs, the question remains as to whether the detection of retinopathy by physicians of other levels of experience can be improved utilizing this method. An interesting analysis of this question is presented in a study from Newcastle,26 which compared nonmydriatic photography, utilizing a camera set up in a mobile unit, with dilated ophthalmoscopy in 2159 patients (4312 eyes) in six clinical settings. Five levels of physicians participated, from house officers to senior consultants; their detection rates for maculopathy and neovascularization are noteworthy. Of 40 eyes with neovascularization later confirmed by an ophthalmologic consultant, ophthalmoscopy identified 9 (22.5%), whereas camera screening identified 14 (35%). Similarly, camera screening was able to identify maculopathy in 45% of confirmed cases, versus 39% by ophthalmoscopy. These findings were consistent regardless of the level of physician, but most striking at the lowest levels of experience, with more high-risk lesions detected by photography than by ophthalmoscopy, suggesting that photography, particularly in less experienced hands, is at least as good as ophthalmoscopy with mydriasis, in the same hands, for detection of neovascularization, and better for detection of maculopathy. COMPARISONS WITH OTHER “PHOTOGRAPHIC” METHODS The question of how many photographic fields are necessary for adequate detection of retinopathy is central to the issue of nonmydriatic fundus photography, and was, in part, investigated during the Wisconsin Epidemiologic Study of Diabetic Retinopathy (WESDR).27 Standard photographic protocols include stereoscopic photography of seven overlapping fields in each eye, to provide views of the optic disc, macula, and adjacent peripheral areas of the retina. In the WESDR, all participants underwent this standard evaluation, their photographs then graded as to degree of retinopathy according to an established algo-
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rithm. Similarly, this algorithm was also utilized to grade retinopathy in a subsample of selected combinations of two, three, or four retinal fields. Severity of retinopathy was broadly categorized into four levels: no retinopathy, mild background retinopathy, moderate background retinopathy, and proliferative retinopathy. The results from the evaluation and classification of 2410 eyes follow. Agreement between the retinopathy level based on seven standard fields and the combinations of fewer fields was 85%, 93%, 95%, and 95%, for two, three, and four fields, respectively. Importantly, the sensitivity of fewer fields, that is, the proportion of eyes with retinopathy that was detected in this manner compared with that detected by the standard seven fields, was relatively high: any retinopathy was detected by two, three, or four fields with sensitivities of 87%, 92%, and 95%, respectively. Sensitivities for detecting proliferative retinopathy were 74%, 86%, and 90%, respectively. No data were presented for detection of retinopathy using a single field, as the nonmydriatic fundus photograph provides. In response to concerns that the single-view photograph taken with the nonmydriatic fundus camera may miss important peripheral lesions, the group from Wales performed a study comparing the usual Polaroid photographs, as well as 35-mm transparencies taken with the same camera through dilated pupils, to fluorescein angiogramsz5 (Note: no information is given regarding the method by which the transparencies were examined.) A high proportion of the Polaroids were unusable (17% versus 2.4% for 35-mm slides). However, comparing the Polaroids and 35mm transparencies of similar quality, of 43 eyes identified to have any retinopathy by fluorescein angiography, 32 (74.4%) were identified by Polaroid photographs and 38 (88.4%) by 35-mm slides. When the retinopathy was classified according to severity, the Polaroid prints also compared well for background retinopathy: it was detected in 26 eyes by fluorescein angiography, 30 eyes by 35-mm transparency, and 25 eyes by the nonmydriatic photographs. Neither photographic technique was comparable to fluorescein angiography for detection of preproliferative retinopathy or macular edema: each identified 5 eyes in this category versus 12 for angiography. The number of eyes with proliferative lesions, i.e., neovascularization, was too small (n = 2) for any definite conclusions regarding efficacy in this category, but both were missed by the Polaroid photography. It should not be surprising, however, that the nonmydriatic photographic technique would be inferior to fluorescein angiography for detection of retinopathy, as the latter is not a “screening” test, but is a sophisticated diagnostic procedure with specific indications. One of the few studies done in the United States,
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from the University of Wisconsin, also compared detection of retinopathy by single-field retinal photographs taken with the nomydriatic camera, through both dilated and undilated pupils, to three-field stereoscopic photographs taken through dilated pupils.18 All photographs were classified by masked, experienced “graders” into one of four levels of severity of retinopathy: none; very early nonproliferative (retinal microaneurysms alone); moderate-to-severe nonproliferative [retinal microaneurysms plus other retinal abnormalities such as hemorrhages, hard exudates, cotton-wool spots, venous beading, or intraretinal microvascular abnormalities (IRMA)]; or proliferative (fibrous proliferation, retinal new vessels, or preretinal or vitreous hemorrhage). For all four grades of severity, exact agreement between gradings of retinopathy of the nondilated single-field photographs and the three-field photographs was 82.5% (n = 63), and 86.5% (n = 74) for the single-field photographs taken through dilated pupils. These data suggest that photographs taken with the nonmydriatic fundus camera, whether through dilated or undilated pupils, are a reasonably reliable means of grading severity of retinopathy, compared with three-field stereoscopic photography. For further comparison, the three-field stereoscopic photographs were compared with direct nonmydriatic ophthalmoscopic examinations, performed by experienced ophthalmic technicians. Exact agreement between gradings of retinopathy for three levels of severity (none, nonproliferative, proliferative) between direct ophthalmoscopy and the steroscopic photographs was only 54.3% (n = 94). Again, this study supports the superiority of nonmydriatic fundus photography for detection of retinopathy over the ophthalmoscopic exam performed without mydriasis. An interesting look at this method comes from another British study, in which Ektachrome slides taken with a nonmydriatic fundus camera were produced in addition to the usual Polaroid prints.28 The detection rates of retinopathy for each were compared, with the slides being both projected onto a white screen and viewed through a macroscope. A total of 66 Polaroids and Ektachrome slides were obtained from 42 type II diabetic patients with nonproliferative retinopathy diagnosed by previous ophthalmoscopic examination. The results demonstrated that the detection of retinal lesions was best for the projected slides and worst for the photographs: the Polaroids revealed only 47% of total hemorrhages and aneurysms, 43% of hard exudates, 73% of macular edema, 73% of IRMA, and 58% of cotton-wool exudates that were identified on the projected slides. The method of viewing the slides was found to be important, in that inspection through the macroscope revealed 74% of total hemorrhages and aneurysms, 67% of hard exu-
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dates, 97% of macular edema, 92% of IRMA, and 86% of cotton-wool exudates that were identified on the projected Ektachromes. The authors suggest that the increase in magnification in addition to the ability to view the full field at once may be reasons for the higher detection rate of the projected slides over either of the other two methods. A minor disadvantage to this method is the special equipment, time, and setting needed to view the slides in this manner. NONMYDRIATIC FUNDUS PHOTOGRAPHY THROUGH DILATED PUPILS As mentioned above, the study from the University of Wisconsin compared fundus photographs taken with the nonmydriatic camera through both undilated and pharmacologically dilated pupils, and found comparable results in detection of retinopathy compared with each other, and with stereoscopic three-field photographs, and much better results than with direct ophthalmoscopy through nondilated pupi1s.l’ Investigators in South Africaz4 similarly compared photographs taken with the nonmydriatic camera under both pupillary conditions in 86 black diabetic patients (172 eyes), with direct ophthalmoscopy with mydriasis, performed by several levels of physicians. Agreement between ophthalmoscopy and photography was not significantly altered by the state of the pupils: 107 eyes were identified as having retinopathy prior to dilation, and 98 eyes after. In a total of 37 eyes, diabetic retinopathy could not be detected on the photographs but was identified by ophthalmoscopy through dilated pupils. However, the authors were of the opinion that “diabetic retinopathy was grossly overdiagnosed by ophthalmoscopy after dilation of the pupils”, perhaps due to difficulty in examining the highly pigmented retinas of black patients. No followup on these patients is offered. The most important finding of this study was a significant improvement in photographs of good quality after (86.6%) versus before (54.7%) dilation. Their conclusion, that photography through a dilated pupil was “superior” to nonmydriatic fundus photography, does not appear to be substantiated by their data as presented, except as relating to the issue of good versus poor quality photographs. Two other studies which have examined accuracy of nonsteroscopic fundus photography through dilated pupils are mentioned for completeness. The retinas of 154 patients with type II diabetes were examined for retinopathy by slit-lamp enhanced by a 60D lens, which provides a high degree of magnification, and by nonstereoscopic retinal photographs taken of two fields of the posterior pole.29 The sensitivity of the photographic method was 87%/97% (right eye/left eye) for detecting background retinopathy and 81%/ 80% for maculopathy, versus 69%/61% and 79%/63%,
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respectively, with the slit-lamp technique (calculated based on the estimated true proportion of eyes with retinopathy and assuming negligible false positives). The authors concluded that the photographic method was not only superior in detecting retinopathy, but much more time efficient; only 5 or 6 patients could be examined per hour with the slit-lamp compared to 30-35 examined by reading retinal photographs. This same group of investigators evaluated 135 diabetic patients who had previously undergone panretinal photocoagulation using these same two methods, and found no significant difference in the two techniques for detecting fibrovascular lesions.30 The issue of using mydriasis can be summarized as follows: it improves the quality of photographs and, therefore, may be valuable in improving the yield from any nonstereoscopic photographic technique. SUMMARY AND CONCLUSIONS To summarize the data, fundus photography with the nonmydriatic camera compares well to other methods of screening for treatable diabetic retinopathy. Its advantages are its relative ease of usage, acceptance by patients, potentially relative low cost, and minimal time expenditure to obtain the photographs. Less often cited, but perhaps equally as important, are the facts that (1) fundus photography provides a static field for examination, and (2) gives a photographic record of the condition of the retina, important in terms of followup, either to document progression of disease or response to treatment or intervention. The photographic record may be useful in epidemiologic studies as well, and its potential benefit for educational purposes is obvious. Its use may also be practical and efficacious in the busy clinic setting or in situations where those caring for diabetic patients are not highly skilled in ophthalmoscopy. Its advantages are further enhanced when certain conditions exist: (1) the photographer is well trained and experienced in the use of the camera; (2) the “readers” are highly qualified, e.g., experienced ophthalmologists or diabetologists; (3) slides are produced for better magnification; and (4) perhaps, pharmacological mydriasis is used. More studies specifically addressing this issue, i.e., comparing photography with the nonmydriatic fundus camera with and without mydriasis, would be informative as to this last point. One of its drawbacks includes difficulty in photographing some patients: those who are unable to cooperate, those with cataracts, those with autonomic neuropathy and poor “natural” pupillary mydriasis. These conditions, in addition to technical failures, contribute to a fairly high rate of unreadable, unusable photographs in some studies. Peripheral retinal lesions may be missed, which may be important in some situations. By and large, however, most high-
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risk retinopathy that requires referral for treatment will occur in the areas of the macula and optic disc, which the single-field photograph covers. Obviously, periodic exams will still be necessary to detect glaucoma and cataracts. Additionally, it should be kept in mind that nonmydriatic fundus photography is not intended to replace more sophisticated evaluations of retinopathy, when indicated. If a significant abnormality is found by fundus photography, or any other screening method, for that matter, it should prompt an appropriate referral for further ophthalmologic evaluation, including fluorescein angiography and or stereoscopic photography, as appropriate. Analysis of the projected costs of using nonmydriatic fundus photography as part of an ongoing program for detection of diabetic retinopathy are favorable, not only when compared with the total lifetime costs of caring for the young onset diabetic patient who loses sight from diabetic eye disease, but also compared with other methods of detection.16 More importantly, it is estimated that biannual screening with nonmydriatic fundus photography could save an estimated 245 sight years in the cohort of patients with younger onset of diabetes.16 A definition of screening as suggested by the European Retinopathy Working Partya is “a simple diagnostic procedure applied to a whole population at risk in order to detect lesions that should be further investigated and treated. It is not a complete clinical assessment but a method to identify patients at risk who will require further examination.” The ideal screening test, then, is quick, easy, cheap, and available, and designed to detect those patients at risk for having the disease or condition for which the screening is being done, without missing a significant proportion; that is, a test which is highly sensitive and has few false negatives. Nonmydriatic fundus photography appears to fulfill many of these qualifications. The real question is will nonmydriatic fundus photography help to detect early treatable diabetic retinopathy better than the average physician using ophthalmoscopy with mydriasis? On this, the verdict is, I believe, still out, although several studies would suggest that it will. Further study is warranted in evaluating its usefulness in the widespread detection of this potentially very treatable, debilitating complication of this very prevalent disease. REFERENCES American College of Physicians, American Diabetes Association, American Academy of Ophthalmology: Screening guidelines for diabetic retinopathy. Ann Intern Med 1992;116:683-685. Singer DE, Nathan DM, Fogel HA, Schachat Al’: Screening for diabetic retinopathy. Ann Intern Med 1992;116:660-671. The Diabetic Retinopathy Study Research Group: Pre-
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liminary report on effects of photocoagulation therapy. Am J Ophthalmol 1976;81:383-396. Early Treatment Diabetic Retinopathy Study Research Group: Photocoagulation for diabetic macular edema: Early Treatment Diabetic Retinopathy Study report number 1. Arch Ophthalmol 1985;103:1796-1806. Javitt JC, Canner JK, Frank RG, Steinwachs DM, Sommer A: Detecting and treating retinopathy in patients with type I diabetes mellitus. Ophthalmology 1990;97: 483-495. Stross JK, Harlan WR: The dissemination of new medical information. JAMA 1979;241:2622-2624. Edwards AL: Funduscopic examination of patients with diabetes who are admitted to the hospital. Canadian Medical Association Journal 1986;134:1263-1265. Sussman EJ, Tsiaras WG, Soper KA: Diagnosis of diabetic eye disease. ]AMA 1982;247:3231-3234. Awh CC, Cupples HW, Javitt JC: Improved detection and referral of patients with diabetic retinopathy by primary care physicians. Arch Intern Med 1991;151: 1405-1408. Nathan DM, Fogel HA, Godine JE, Lou PL, D’Amico DJ, Regan CDJ, Topping TM: Role of diabetologist in evaluating diabetic retinopathy. Diabetes Cure 1991;14: 26-33. Rogers D, Bitner-Glindzicz M, Harris C, Yudkin JS: Non-mydriatic retinal photography as a screening service for general practitioners. Diabetic Med 1990;7: 165-167. Adamson E, Herman W: Patterns of medical care for diabetics in the San Francisco Bay Area. Atlanta, GA: Diabetes Translational Program, Centers for Disease Control, 1988. Jones RB, Larizgoitia I, Casado L, Barrie T: How effective if the referral chain for diabetic retinopathy? Diubetic Med 1989;6:262-266. Klein R, Klein BEK, Moss SE, Davis MD, DeMets DL: The Wisconsin epidemiologic study of diabetic retinopathy, VI: Retinal photocoagulation. Ophthalmology 1987;94:747-753. Witkin SR, Klein R: Ophthalmologic care for persons with diabetes. JAMA 1984;251:2534-2537. Dasbach EJ, Fryback DG, Newcomb PA, Klein R, Klein BEK: Cost-effectiveness of strategies for detecting diabetic retinopathy. Med Care 1991;29:20-39. Leese GP, Newton RW, Jung RT, Haining W, Ellingford A, and the Tayside Mobile Eye Screening Unit: Screening for diabetic retinopathy in a widely spaced population using non-mydriatic fundus photography in a mobile unit. Diabetic Med 1992;9:459-462. Klein R, Klein BEK, Neider W, Hubbard LD, Meuer SM, Brothers RJ: Diabetic retinopathy as detected usina onhthalmoscouv. a nonmvdriatic camera and a
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standard fundus camera. Ophthalmology 1985;92: 485-491. Barrie T, MacCuish AC: Assessment of non-mydriatic fundus photography in detection of diabetic retinopathy. BMJ 1986;293:1304-1305. Buxton MJ, Sculpher MJ, Ferguson BA, Humphreys JE, Altman JFB, Spiegelhalter DJ, Kirby AJ, Jacob JS, Bacon H, Dudbridge SB, Stead JW, Feest TG, Cheng H, Franklin SL, Courtney P, Talbot JF, Ahmed R, Dabbs TR: Screening for treatable diabetic retinopathy: A comparison of different methods. Diabetic Med 1991; 41371-377. Williams R, Nussey S, Humphry R, Thompson G: Assessment of non-mydriatic fundus photography in detection of diabetic retinopathy. BMJ 1986;293: 1140-1142. Higgs ER, Harney BA, Kelleher A, Reckless JPD: Detection of diabetic retinopathy in the community using a non-mydriatic camera. Diabetic Med 1991;6:551-555. 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. BMJ 1985;291:1256-1257. Mollentze WF, Stulting AA, Steyn AF: Ophthalmoscopy versus non-mydriatic fundus photography in the detection of diabetic retinopathy in black patients. S Afr Med J 1990;78:248-250. Jones D, Dolben J, Owens DR, Vora JP, Young S, Creagh FM: Non-mydriatic Polaroid phtography in screening for diabetic retinopathy: Evaluation in a dinical setting. BMJ 1988;296:1029-1030. Taylor R, Lovelock L, Tunbridge WMG, Alberti KGMM, Brackenridge RG, Stephenson I’, Young E: Comparison of non-mydriatic retinal photography with ophthalmoscopy in 2159 patients: Mobile retinal camera study. BMJ 1990;301:1243-1247. Moss SE, Meuer SM, Klein R, Hubbard LD, Brothers RJ, Klein BEK: Are seven standard photographic fields necessary for classification of diabetic retinopathy? lnvest Ophthalmol Vis Sci 1989;30:823-838. Pardhan S, Gilchrist J: Comparison of non-stereo polaroids and slides in detection of diabetic retinopathy. Actu Ophthalmol 1991;69:586-590. Kalm H, Egertsen R, Blohme G: Non-stereo fundus photography as a screening procedure for diabetic retinopathy among patients with type II diabetes. Actu Ophthalmol 1989;67:546-553. Kalm H, Sjodell L, Jonsson R: Non-stereo photographic screening after panretinal photocoagulation for proliferative diabetic retinopathy. Actu Ophthalmol 1989;67:554-559. Retinopathy Working Party: A protocol for screening for diabetic retinopathy in Europe. Diabetic Med 1991; 8:263-267.
Nonmydriatic Fundus Photography in Screening for Treatable Diabetic Retinopathy ]ennifer B. Marks
ABSTRACT Diabetic retinopathy is a complication of both insulin-dependent (type I1 and non-insulindependent (type II) diabetes. The American Diabetes Association and others recommend screening for retinopathy, beginning 5 years after onset of symptoms for patients with type I diabetes and at the time of diagnosis for patients with type II diabetes. Ideally, diabetic patients are evaluated at recommended intervals by an ophthalmologist. Realistically, however, this is often not feasable, for reasons both of cost and availability. There is evidence that many diabetic patients are being referred too late for intervention, perhaps in part due to lax screening and detection, often the responsibility of internists and other primary care physicians. Data supports
the need for a cheap, widely available, easy-to-use, effective screening tool for detecting treatable diabetic retinopathy. To this end, several studies have evaluated nonmydriatic fundus photography, and compared it with more-established methods of detecting diabetic retinal disease. The real question to be considered is whether nonmydriatic fundus photography will help to detect early treatable retinopathy better than the average physician using ophthalmoscopy. Several studies support its usefulness in this regard, and are discussed in this review. Questions remain, however, and further study is warranted in evaluating its potential role. (Journal of Diabetes and Its Complications, 6;4:247-253, 1992.1
INTRODUCTION
or advanced proliferative retinopathy. It is of importance that many patients at high risk for visual loss are asymptomatic. Therefore, the American Diabetes Association and other&* recommend screening for retinopathy, beginning 5 years after onset of symptoms for patients with type I diabetes and at the time of diagnosis for patients with type II diabetes. Screening strategies and recommendations are based on the fact that, in general, the development and progression of diabetic retinopathy is orderly, advancing from mild background abnormalities through a preproliferative to a proliferative stage, each characterized by retinal changes which can be recognized and, when appropriate, treated. The results of several different randomized trials3f4 have clearly established the efficacy of laser treatment in preserving vision in diabetic patients with proliferative retinopathy and macular edema and more than justify screening for this complication.
iabetic retinopathy is a complication of both insulin-dependent (type I) and non-insulin-dependent (type II) diabetes. By 20 years duration of disease, nearly all type I and more than 60% of type II diabetic patients have some degree of retinopathy. Despite the availability of effective treatment, it remains the leading cause of blindness in working-age adults in industrialized countries. Visual loss results from either maculopathy
D
From the Department of Medicine, Division of Endocrinology, University of Miami School of Medicine, Miami, Florida, USA. Reprint requests to be sent to: Dr. Jennifer B. Marks, Department of Medicine, Division of Endocrinology, University of Miami School of Medicine, 1500 NW 12 Avenue, Jackson Medical Towers, Miami, FL 33136. 0 1992 ]ournal of Diabetes and Its Complications
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In the ideal world, diabetic patients are evaluated at recommended intervals by an ophthalmologist. Realistically, however, this is often not feasable, for reasons of both cost and availability. Office examinations of this nature are often not covered by Medicare or private insurance carriers. Moreover, it has been estimated that 8% of patients with diabetes mellitus in the United States have no health insurance.5 Screening is therefore left to physicians who may or may not understand the importance of detecting treatable retinopathy, possess the skill to identify significant retinopathy by direct ophthalmoscopic exam, or be aware of the indications for referral for treatment.6,7 Indeed, diabetologists and general internists have been shown to misdiagnose serious retinal lesions when performing direct ophthalmoscopy through a dilated pupil’ although with motivation, this skill can be imtraining, and experience, proved.9,*0 Data suggest that many primary care physicians do not even include ophthalmoscopy as part of the routine examination of their diabetic patients,9,11,12 and even less frequentIy utilize mydriasis9,12 Moreover, there is evidence that many diabetic patients are being referred too late for intervention,
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perhaps in part due to lax screening and detection.13-*5 There exists, therefore, a need for a cheaper, widely available, easy-to-use, effective screening tool for detecting treatable diabetic retinopathy. To this end, several studies have evaluated nonmydriatic fundus photography, and compared it with more-established methods of detecting diabetic retinal disease. Despite ongoing controversy regarding its effectiveness in identifying high-risk lesions, its clinical use is increasing, and it is being advocated a a method for screening for diabetic retinopathy.16,17 USE OF THE NONMYDRIATIC FUNDUS CAMERA The nonmydriatic fundus camera provides an instant color photograph, on Polaroid film, of a 45-degree field of the retina, including the macula and the optic disc, through an undilated pupil (Figure 1). The first eye is photographed after approximately 5 min of adaptation in a darkened room; the second, 5-10 min later, to allow the pupils time to dilate after the first flash. Data suggest that the procedure is well tolerated by patients,l’,‘* and the camera is relatively easy to use.l*
FIGURE 1 Polaroid photograph of a 45-degree field of a normal retina ~ taken with the Canon nonmydriatic ’ fundus camera, showing the macula and the optic disc.
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Technical problems, however, are not infrequently encountered. Difficulty in obtaining photographs of good quality may occur as a result of many factors. Camera failure, i.e., failure of flash, was responsible for loss of approximately 30% of photographs in one study. I8 Lens opacities or cataracts, and inadequate pupillary mydriasis occur to a variable degree, particularly in more elderly populations with long duration of disease.1s,19 Artifacts and inexact focusing are other problems that may result in unsatisfactory photographs. I8 In studies evaluating the quality of photographs, the percentage of those that are unusable varies, and may range from as low as 4%-6%17,20,21 to as high as 22% -25%. 22,23This percentage may be somewhat lower if photographs are taken through a pharmacologically dilated pupil. *8,24,25 Several studies have compared the accuracy of nonmydriatic photography with various other methods to detect diabetic retinopathy, including direct and indirect ophthalmoscopy through both undilated and pharmacologically dilated pupils, stereoscopic photography, and fluorescein angiography. EFFICACY OF THE NONMYDRIATIC CAMERA FOR DETECTING SIGNIFICANT RETINOPATHY-COMPARISONS WITH OPHTHALMOSCOPY A study from the University Hospital of Wales23 evaluated the ability of physicians in a busy diabetic clinic to identify retinopathy by direct ophthalmoscopic examination through both dilated and undilated pupils, compared with detection of retinopathy by photographs taken with the nonmydriatic fundus camera. Of 137 eyes studied, the physicians found 24 with diabetic retinopathy present by photograph, whereas only 2 of those eyes had been identified by examination through undilated pupils, and only 8 through dilated pupils. In a repeat trial, the physicians achieved marginally better results. Of 90 eyes studied, 21 showed diabetic retinopathy on the photographs, whereas only 9 of those were detected by ophthalmoscopy through undilated pupils and only 8 through dilated pupils. That is, the photographs identified 23% of eyes as having some degree of retinopathy, while direct examination through undilated and dilated pupils identified 10% and 13%, respectively; a striking difference in detection rate. The authors concluded from this data that nonmydriatic fundus photography is an effective means of increasing the rate of identification of diabetic retinopathy in a busy diabetic clinic where ophthalmoscopy is overlooked or performed in a hurried manner. Other studies in similar clinical settings have found similar results,11,22,26but unfortunately provide no information regarding the actual efficacy of the technique in question, only showing it to be superior when compared with subop-
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timal ophthalmologic exams. In certain situations, of course, this may be important. In Britain, the Health Economics Research Group2’ evaluated 6304 eyes of 3318 diabetic patients in three general diabetic clinics using nonmydriatic fundus photography. Photographs were taken by specially trained ophthalmologic assistants and evaluated by hospital-based physicians and community general practitioners. Their diagnoses compared favorably to the diagnoses made by ophthalmologic exam performed by ophthalmologic opticians through dilated pupils. The sensitivities of all three techniques for detecting either proliferative retinopathy or maculopathy, however, were low (67% and 53% for photographs versus 47% for exams), despite a large proportion of fair-to-excellent quality photos (76%). These globally poor rates of detection are more likely a reflection of the lack of knowledge, experience, and/ or skills of the examiners, rather than the efficacy of nonmydriatic fundus photography, to detect retinopathy. The authors readily admit the lack of a ‘gold standard’ in this study, with exams performed by opticians being the reference standard for comparison to photographic results. Researchers at St. George’s Hospital in London*l also compared nonmydriatic fundus photography to ophthalmoscopy, but an experienced ophthalmologist performed the direct and indirect examinations through dilated pupils, a higher standard for comparison than that of either of the previous two studies. The photographs were also interpreted by more qualified readers, two ophthalmologists who were masked to the results of their colleague’s examinations. The results showed that the percentage of eyes identified as having three broad categories of retinopathy on the photographs compared favorably with the ophthalmologist’s diagnoses by examination: any retinopathy (58% versus 60%, respectively), maculopathy (27% for each), and neovascularization (7.5% versus 6.7%). Ophthalmoscopy identified retinopathy in 71 of 120 eyes; this was detected by the camera with an overall sensitivity of 96%, a specificity of 98%, a false negative rate of 6.8%, and false positive rate of 2%. The sensitivities and specificities for detecting maculopathy (n = 32) and neovascularization (n = 11) were 100% and 96%, and 82% and lOO%,respectively. Using this data and an approximate prevalence of retinopathy in a general diabetic clinic of lo%, the positive and negative predictive values are calculated to be 84% and 99.5%, respectively. That is, if retinopathy was identified on the photographs, it was 84% likely to be correct, whereas if retinopathy was not identified, it was 99.5% likely to be correct. In essence, then, based on these data, nonmydriatic fundus photography should detect most retinopathy, and, with such high specificity, would falsely identify few normal eyes as having
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retinopathy, thus wasting little money on unnecessary referrals for further evaluation or intervention. The authors’ conclusion, that nonmydriatic fundus photography, with later interpretation of photographs by an ophthalmologist, is an effective screening method for detection of diabetic retinopathy, would appear valid. The results of this study, however, have been criticized as being at variance with the experience of others. I9 A reasonable concern is that photographs taken with the nonmydriatic fundus camera miss important retinal lesions, particularly in the peripheral retina, which the camera does not photograph, or in the eyes of patients with small pupils or lens opacities. As not all clinical settings will have an opthalmologist available for interpretation of nonmydriatic photographs, the question remains as to whether the detection of retinopathy by physicians of other levels of experience can be improved utilizing this method. An interesting analysis of this question is presented in a study from Newcastle,26 which compared nonmydriatic photography, utilizing a camera set up in a mobile unit, with dilated ophthalmoscopy in 2159 patients (4312 eyes) in six clinical settings. Five levels of physicians participated, from house officers to senior consultants; their detection rates for maculopathy and neovascularization are noteworthy. Of 40 eyes with neovascularization later confirmed by an ophthalmologic consultant, ophthalmoscopy identified 9 (22.5%), whereas camera screening identified 14 (35%). Similarly, camera screening was able to identify maculopathy in 45% of confirmed cases, versus 39% by ophthalmoscopy. These findings were consistent regardless of the level of physician, but most striking at the lowest levels of experience, with more high-risk lesions detected by photography than by ophthalmoscopy, suggesting that photography, particularly in less experienced hands, is at least as good as ophthalmoscopy with mydriasis, in the same hands, for detection of neovascularization, and better for detection of maculopathy. COMPARISONS WITH OTHER “PHOTOGRAPHIC” METHODS The question of how many photographic fields are necessary for adequate detection of retinopathy is central to the issue of nonmydriatic fundus photography, and was, in part, investigated during the Wisconsin Epidemiologic Study of Diabetic Retinopathy (WESDR).27 Standard photographic protocols include stereoscopic photography of seven overlapping fields in each eye, to provide views of the optic disc, macula, and adjacent peripheral areas of the retina. In the WESDR, all participants underwent this standard evaluation, their photographs then graded as to degree of retinopathy according to an established algo-
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rithm. Similarly, this algorithm was also utilized to grade retinopathy in a subsample of selected combinations of two, three, or four retinal fields. Severity of retinopathy was broadly categorized into four levels: no retinopathy, mild background retinopathy, moderate background retinopathy, and proliferative retinopathy. The results from the evaluation and classification of 2410 eyes follow. Agreement between the retinopathy level based on seven standard fields and the combinations of fewer fields was 85%, 93%, 95%, and 95%, for two, three, and four fields, respectively. Importantly, the sensitivity of fewer fields, that is, the proportion of eyes with retinopathy that was detected in this manner compared with that detected by the standard seven fields, was relatively high: any retinopathy was detected by two, three, or four fields with sensitivities of 87%, 92%, and 95%, respectively. Sensitivities for detecting proliferative retinopathy were 74%, 86%, and 90%, respectively. No data were presented for detection of retinopathy using a single field, as the nonmydriatic fundus photograph provides. In response to concerns that the single-view photograph taken with the nonmydriatic fundus camera may miss important peripheral lesions, the group from Wales performed a study comparing the usual Polaroid photographs, as well as 35-mm transparencies taken with the same camera through dilated pupils, to fluorescein angiogramsz5 (Note: no information is given regarding the method by which the transparencies were examined.) A high proportion of the Polaroids were unusable (17% versus 2.4% for 35-mm slides). However, comparing the Polaroids and 35mm transparencies of similar quality, of 43 eyes identified to have any retinopathy by fluorescein angiography, 32 (74.4%) were identified by Polaroid photographs and 38 (88.4%) by 35-mm slides. When the retinopathy was classified according to severity, the Polaroid prints also compared well for background retinopathy: it was detected in 26 eyes by fluorescein angiography, 30 eyes by 35-mm transparency, and 25 eyes by the nonmydriatic photographs. Neither photographic technique was comparable to fluorescein angiography for detection of preproliferative retinopathy or macular edema: each identified 5 eyes in this category versus 12 for angiography. The number of eyes with proliferative lesions, i.e., neovascularization, was too small (n = 2) for any definite conclusions regarding efficacy in this category, but both were missed by the Polaroid photography. It should not be surprising, however, that the nonmydriatic photographic technique would be inferior to fluorescein angiography for detection of retinopathy, as the latter is not a “screening” test, but is a sophisticated diagnostic procedure with specific indications. One of the few studies done in the United States,
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from the University of Wisconsin, also compared detection of retinopathy by single-field retinal photographs taken with the nomydriatic camera, through both dilated and undilated pupils, to three-field stereoscopic photographs taken through dilated pupils.18 All photographs were classified by masked, experienced “graders” into one of four levels of severity of retinopathy: none; very early nonproliferative (retinal microaneurysms alone); moderate-to-severe nonproliferative [retinal microaneurysms plus other retinal abnormalities such as hemorrhages, hard exudates, cotton-wool spots, venous beading, or intraretinal microvascular abnormalities (IRMA)]; or proliferative (fibrous proliferation, retinal new vessels, or preretinal or vitreous hemorrhage). For all four grades of severity, exact agreement between gradings of retinopathy of the nondilated single-field photographs and the three-field photographs was 82.5% (n = 63), and 86.5% (n = 74) for the single-field photographs taken through dilated pupils. These data suggest that photographs taken with the nonmydriatic fundus camera, whether through dilated or undilated pupils, are a reasonably reliable means of grading severity of retinopathy, compared with three-field stereoscopic photography. For further comparison, the three-field stereoscopic photographs were compared with direct nonmydriatic ophthalmoscopic examinations, performed by experienced ophthalmic technicians. Exact agreement between gradings of retinopathy for three levels of severity (none, nonproliferative, proliferative) between direct ophthalmoscopy and the steroscopic photographs was only 54.3% (n = 94). Again, this study supports the superiority of nonmydriatic fundus photography for detection of retinopathy over the ophthalmoscopic exam performed without mydriasis. An interesting look at this method comes from another British study, in which Ektachrome slides taken with a nonmydriatic fundus camera were produced in addition to the usual Polaroid prints.28 The detection rates of retinopathy for each were compared, with the slides being both projected onto a white screen and viewed through a macroscope. A total of 66 Polaroids and Ektachrome slides were obtained from 42 type II diabetic patients with nonproliferative retinopathy diagnosed by previous ophthalmoscopic examination. The results demonstrated that the detection of retinal lesions was best for the projected slides and worst for the photographs: the Polaroids revealed only 47% of total hemorrhages and aneurysms, 43% of hard exudates, 73% of macular edema, 73% of IRMA, and 58% of cotton-wool exudates that were identified on the projected slides. The method of viewing the slides was found to be important, in that inspection through the macroscope revealed 74% of total hemorrhages and aneurysms, 67% of hard exu-
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dates, 97% of macular edema, 92% of IRMA, and 86% of cotton-wool exudates that were identified on the projected Ektachromes. The authors suggest that the increase in magnification in addition to the ability to view the full field at once may be reasons for the higher detection rate of the projected slides over either of the other two methods. A minor disadvantage to this method is the special equipment, time, and setting needed to view the slides in this manner. NONMYDRIATIC FUNDUS PHOTOGRAPHY THROUGH DILATED PUPILS As mentioned above, the study from the University of Wisconsin compared fundus photographs taken with the nonmydriatic camera through both undilated and pharmacologically dilated pupils, and found comparable results in detection of retinopathy compared with each other, and with stereoscopic three-field photographs, and much better results than with direct ophthalmoscopy through nondilated pupi1s.l’ Investigators in South Africaz4 similarly compared photographs taken with the nonmydriatic camera under both pupillary conditions in 86 black diabetic patients (172 eyes), with direct ophthalmoscopy with mydriasis, performed by several levels of physicians. Agreement between ophthalmoscopy and photography was not significantly altered by the state of the pupils: 107 eyes were identified as having retinopathy prior to dilation, and 98 eyes after. In a total of 37 eyes, diabetic retinopathy could not be detected on the photographs but was identified by ophthalmoscopy through dilated pupils. However, the authors were of the opinion that “diabetic retinopathy was grossly overdiagnosed by ophthalmoscopy after dilation of the pupils”, perhaps due to difficulty in examining the highly pigmented retinas of black patients. No followup on these patients is offered. The most important finding of this study was a significant improvement in photographs of good quality after (86.6%) versus before (54.7%) dilation. Their conclusion, that photography through a dilated pupil was “superior” to nonmydriatic fundus photography, does not appear to be substantiated by their data as presented, except as relating to the issue of good versus poor quality photographs. Two other studies which have examined accuracy of nonsteroscopic fundus photography through dilated pupils are mentioned for completeness. The retinas of 154 patients with type II diabetes were examined for retinopathy by slit-lamp enhanced by a 60D lens, which provides a high degree of magnification, and by nonstereoscopic retinal photographs taken of two fields of the posterior pole.29 The sensitivity of the photographic method was 87%/97% (right eye/left eye) for detecting background retinopathy and 81%/ 80% for maculopathy, versus 69%/61% and 79%/63%,
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respectively, with the slit-lamp technique (calculated based on the estimated true proportion of eyes with retinopathy and assuming negligible false positives). The authors concluded that the photographic method was not only superior in detecting retinopathy, but much more time efficient; only 5 or 6 patients could be examined per hour with the slit-lamp compared to 30-35 examined by reading retinal photographs. This same group of investigators evaluated 135 diabetic patients who had previously undergone panretinal photocoagulation using these same two methods, and found no significant difference in the two techniques for detecting fibrovascular lesions.30 The issue of using mydriasis can be summarized as follows: it improves the quality of photographs and, therefore, may be valuable in improving the yield from any nonstereoscopic photographic technique. SUMMARY AND CONCLUSIONS To summarize the data, fundus photography with the nonmydriatic camera compares well to other methods of screening for treatable diabetic retinopathy. Its advantages are its relative ease of usage, acceptance by patients, potentially relative low cost, and minimal time expenditure to obtain the photographs. Less often cited, but perhaps equally as important, are the facts that (1) fundus photography provides a static field for examination, and (2) gives a photographic record of the condition of the retina, important in terms of followup, either to document progression of disease or response to treatment or intervention. The photographic record may be useful in epidemiologic studies as well, and its potential benefit for educational purposes is obvious. Its use may also be practical and efficacious in the busy clinic setting or in situations where those caring for diabetic patients are not highly skilled in ophthalmoscopy. Its advantages are further enhanced when certain conditions exist: (1) the photographer is well trained and experienced in the use of the camera; (2) the “readers” are highly qualified, e.g., experienced ophthalmologists or diabetologists; (3) slides are produced for better magnification; and (4) perhaps, pharmacological mydriasis is used. More studies specifically addressing this issue, i.e., comparing photography with the nonmydriatic fundus camera with and without mydriasis, would be informative as to this last point. One of its drawbacks includes difficulty in photographing some patients: those who are unable to cooperate, those with cataracts, those with autonomic neuropathy and poor “natural” pupillary mydriasis. These conditions, in addition to technical failures, contribute to a fairly high rate of unreadable, unusable photographs in some studies. Peripheral retinal lesions may be missed, which may be important in some situations. By and large, however, most high-
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risk retinopathy that requires referral for treatment will occur in the areas of the macula and optic disc, which the single-field photograph covers. Obviously, periodic exams will still be necessary to detect glaucoma and cataracts. Additionally, it should be kept in mind that nonmydriatic fundus photography is not intended to replace more sophisticated evaluations of retinopathy, when indicated. If a significant abnormality is found by fundus photography, or any other screening method, for that matter, it should prompt an appropriate referral for further ophthalmologic evaluation, including fluorescein angiography and or stereoscopic photography, as appropriate. Analysis of the projected costs of using nonmydriatic fundus photography as part of an ongoing program for detection of diabetic retinopathy are favorable, not only when compared with the total lifetime costs of caring for the young onset diabetic patient who loses sight from diabetic eye disease, but also compared with other methods of detection.16 More importantly, it is estimated that biannual screening with nonmydriatic fundus photography could save an estimated 245 sight years in the cohort of patients with younger onset of diabetes.16 A definition of screening as suggested by the European Retinopathy Working Partya is “a simple diagnostic procedure applied to a whole population at risk in order to detect lesions that should be further investigated and treated. It is not a complete clinical assessment but a method to identify patients at risk who will require further examination.” The ideal screening test, then, is quick, easy, cheap, and available, and designed to detect those patients at risk for having the disease or condition for which the screening is being done, without missing a significant proportion; that is, a test which is highly sensitive and has few false negatives. Nonmydriatic fundus photography appears to fulfill many of these qualifications. The real question is will nonmydriatic fundus photography help to detect early treatable diabetic retinopathy better than the average physician using ophthalmoscopy with mydriasis? On this, the verdict is, I believe, still out, although several studies would suggest that it will. Further study is warranted in evaluating its usefulness in the widespread detection of this potentially very treatable, debilitating complication of this very prevalent disease. REFERENCES American College of Physicians, American Diabetes Association, American Academy of Ophthalmology: Screening guidelines for diabetic retinopathy. Ann Intern Med 1992;116:683-685. Singer DE, Nathan DM, Fogel HA, Schachat Al’: Screening for diabetic retinopathy. Ann Intern Med 1992;116:660-671. The Diabetic Retinopathy Study Research Group: Pre-
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liminary report on effects of photocoagulation therapy. Am J Ophthalmol 1976;81:383-396. Early Treatment Diabetic Retinopathy Study Research Group: Photocoagulation for diabetic macular edema: Early Treatment Diabetic Retinopathy Study report number 1. Arch Ophthalmol 1985;103:1796-1806. Javitt JC, Canner JK, Frank RG, Steinwachs DM, Sommer A: Detecting and treating retinopathy in patients with type I diabetes mellitus. Ophthalmology 1990;97: 483-495. Stross JK, Harlan WR: The dissemination of new medical information. JAMA 1979;241:2622-2624. Edwards AL: Funduscopic examination of patients with diabetes who are admitted to the hospital. Canadian Medical Association Journal 1986;134:1263-1265. Sussman EJ, Tsiaras WG, Soper KA: Diagnosis of diabetic eye disease. ]AMA 1982;247:3231-3234. Awh CC, Cupples HW, Javitt JC: Improved detection and referral of patients with diabetic retinopathy by primary care physicians. Arch Intern Med 1991;151: 1405-1408. Nathan DM, Fogel HA, Godine JE, Lou PL, D’Amico DJ, Regan CDJ, Topping TM: Role of diabetologist in evaluating diabetic retinopathy. Diabetes Cure 1991;14: 26-33. Rogers D, Bitner-Glindzicz M, Harris C, Yudkin JS: Non-mydriatic retinal photography as a screening service for general practitioners. Diabetic Med 1990;7: 165-167. Adamson E, Herman W: Patterns of medical care for diabetics in the San Francisco Bay Area. Atlanta, GA: Diabetes Translational Program, Centers for Disease Control, 1988. Jones RB, Larizgoitia I, Casado L, Barrie T: How effective if the referral chain for diabetic retinopathy? Diubetic Med 1989;6:262-266. Klein R, Klein BEK, Moss SE, Davis MD, DeMets DL: The Wisconsin epidemiologic study of diabetic retinopathy, VI: Retinal photocoagulation. Ophthalmology 1987;94:747-753. Witkin SR, Klein R: Ophthalmologic care for persons with diabetes. JAMA 1984;251:2534-2537. Dasbach EJ, Fryback DG, Newcomb PA, Klein R, Klein BEK: Cost-effectiveness of strategies for detecting diabetic retinopathy. Med Care 1991;29:20-39. Leese GP, Newton RW, Jung RT, Haining W, Ellingford A, and the Tayside Mobile Eye Screening Unit: Screening for diabetic retinopathy in a widely spaced population using non-mydriatic fundus photography in a mobile unit. Diabetic Med 1992;9:459-462. Klein R, Klein BEK, Neider W, Hubbard LD, Meuer SM, Brothers RJ: Diabetic retinopathy as detected usina onhthalmoscouv. a nonmvdriatic camera and a
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standard fundus camera. Ophthalmology 1985;92: 485-491. Barrie T, MacCuish AC: Assessment of non-mydriatic fundus photography in detection of diabetic retinopathy. BMJ 1986;293:1304-1305. Buxton MJ, Sculpher MJ, Ferguson BA, Humphreys JE, Altman JFB, Spiegelhalter DJ, Kirby AJ, Jacob JS, Bacon H, Dudbridge SB, Stead JW, Feest TG, Cheng H, Franklin SL, Courtney P, Talbot JF, Ahmed R, Dabbs TR: Screening for treatable diabetic retinopathy: A comparison of different methods. Diabetic Med 1991; 41371-377. Williams R, Nussey S, Humphry R, Thompson G: Assessment of non-mydriatic fundus photography in detection of diabetic retinopathy. BMJ 1986;293: 1140-1142. Higgs ER, Harney BA, Kelleher A, Reckless JPD: Detection of diabetic retinopathy in the community using a non-mydriatic camera. Diabetic Med 1991;6:551-555. 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. BMJ 1985;291:1256-1257. Mollentze WF, Stulting AA, Steyn AF: Ophthalmoscopy versus non-mydriatic fundus photography in the detection of diabetic retinopathy in black patients. S Afr Med J 1990;78:248-250. Jones D, Dolben J, Owens DR, Vora JP, Young S, Creagh FM: Non-mydriatic Polaroid phtography in screening for diabetic retinopathy: Evaluation in a dinical setting. BMJ 1988;296:1029-1030. Taylor R, Lovelock L, Tunbridge WMG, Alberti KGMM, Brackenridge RG, Stephenson I’, Young E: Comparison of non-mydriatic retinal photography with ophthalmoscopy in 2159 patients: Mobile retinal camera study. BMJ 1990;301:1243-1247. Moss SE, Meuer SM, Klein R, Hubbard LD, Brothers RJ, Klein BEK: Are seven standard photographic fields necessary for classification of diabetic retinopathy? lnvest Ophthalmol Vis Sci 1989;30:823-838. Pardhan S, Gilchrist J: Comparison of non-stereo polaroids and slides in detection of diabetic retinopathy. Actu Ophthalmol 1991;69:586-590. Kalm H, Egertsen R, Blohme G: Non-stereo fundus photography as a screening procedure for diabetic retinopathy among patients with type II diabetes. Actu Ophthalmol 1989;67:546-553. Kalm H, Sjodell L, Jonsson R: Non-stereo photographic screening after panretinal photocoagulation for proliferative diabetic retinopathy. Actu Ophthalmol 1989;67:554-559. Retinopathy Working Party: A protocol for screening for diabetic retinopathy in Europe. Diabetic Med 1991; 8:263-267.
