The Influence of Age, Duration of Diabetes, Cataract, and Pupil Size on Image Quality in Digital Photographic Retinal Screening PETER HENRY SCANLON, MRCP1 CHRIS FOY, MSC2 RAMAN MALHOTRA, FRCO, PHTH3 STEPHEN J. ALDINGTON, DMS4 OBJECTIVE — To evaluate the effect of age, duration of diabetes, cataract, and pupil size on the image quality in digital photographic screening. RESEARCH DESIGN AND METHODS — Randomized groups of 3,650 patients had one-field, nonmydriatic, 45° digital retinal imaging photography before mydriatic two-field photography. A total of 1,549 patients were then examined by an experienced ophthalmologist. Outcome measures were ungradable image rates, age, duration of diabetes, detection of referable diabetic retinopathy, presence of early or obvious central cataract, pupil diameter, and iris color. RESULTS — The ungradable image rate for nonmydriatic photography was 19.7% (95% CI 18.4 –21.0) and for mydriatic photography was 3.7% (3.1– 4.3). The odds of having one eye ungradable increased by 2.6% (1.6 –3.7) for each extra year since diagnosis for nonmydriatic, by 4.1% (2.7–5.7) for mydriatic photography irrespective of age, by 5.8% (5.0 – 6.7) for nonmyd- riatic, and by 8.4% (6.5–10.4) for mydriatic photography for every extra year of age, irrespective of years since diagnosis. Obvious central cataract was present in 57% of ungradable mydriatic photographs, early cataract in 21%, no cataract in 9%, and 13% had other pathologies. The pupil diameter in the ungradable eyes showed a significant trend (P � 0.001) in the three groups (obvious cataract 4.434, early cataract 3.379, and no cataract 2.750). CONCLUSIONS — The strongest predictor of ungradable image rates, both for nonmydri- atic and mydriatic digital photography, is the age of the person with diabetes. The most common cause of ungradable images was obvious central cataract. Diabetes Care 28:2448 –2453, 2005 T he use of nonmydriatic photogra- phy has been reported from the U.S. (1– 4), Japan (5), Australia (6,7), France (8), and the U.K. (9 –13). Reports of ungradable image rates for nonmydri- atic photography vary between 4% re- ported by Leese et al. (10) and 34% reported by Higgs et al. (13). In the U.K., national screening pro- grams for detection of sight-threatening diabetic retinopathy are being imple- mented in England (14), Scotland (15), Wales, and Northern Ireland. England and Wales are using two 45° field mydri- atic digital photography as their preferred method. Scotland is using a three-stage screening procedure, in which the first stage is one-field nonmydriatic digital photography with mydriatic photography used for failures of nonmydriatic photog- raphy and slit-lamp biomicroscopy for failures of both photographic methods. Northern Ireland is performing nonmyd- riatic photography in those aged �50 years and mydriatic photography in those aged �50 years. The Gloucestershire Diabetic Eye Study (9) was designed to formally eval- uate the community-based nonmydriatic and mydriatic digital photographic screening program that was introduced in October 1998. The current study was de- signed to evaluate the effect of age, dura- tion of diabetes, cataract, and pupil size on the image quality in nonmydriatic and mydriatic digital photographic screening. RESEARCH DESIGN AND METHODS — For the comparison of mydriatic photography and nonmydriatic photography in those patients with grad- able images, the Gloucestershire Diabetic Eye Study (9) was designed to detect a difference of 2% in the detection of refer- able diabetic retinopathy between the methods (9% for mydriatic and 7% for nonmydriatic photography). To detect this difference with 80% power and 5% sig- nificance level, 3,650 patients had to be examined, allowing for an estimated un- gradable image rate of 15% with nonmyd- riatic photography. Eighty groups of 50 patients from within individual general practices were randomly selected for inclu- sion as potential study patients. This num- ber allowed for lower rates of screening uptake within some of the study practices. The patient’s history (including dia- betes type) was taken and signed consent obtained. Patients classified as type 1 had commenced insulin within 4 months of diagnosis, while patients classified type 2 were not requiring insulin or commenced insulin after 4 months of diagnosis. Visual acuity was measured using ret- roilluminated LogMAR charts modified from those used in the Early Treatment Diabetic Retinopathy Study (16). One 45° nonmydriatic digital photograph was taken of each eye using a Topcon NRW5S camera with Sony 950 video camera cen- tered on the macula, repeated once only if necessary. After mydriasis with Tropic- amide 1%, two 45° photographs, macular and nasal, were taken of each eye accord- ing to the EURODIAB protocol (17). Di- rect ophthalmoscopy was performed, the results of which were recorded. The screener was at liberty to take additional retinal or anterior segment views if he ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● From the 1Department of Ophthalmology, Cheltenham General Hospital, Cheltenham, U.K.; the 2R&D Support Unit, Gloucester Hospitals National Health Service Trust, Gloucester, U.K.; the 3Oxford Eye Hos- pital, Oxford, U.K.; and the 4Retinopathy Grading Centre, Imperial College, London, U.K. Address correspondence and reprint requests to Dr. Peter Scanlon, Gloucestershire Eye Unit, Cheltenham General Hospital, Sandford Road, Cheltenham, GL53 7AN, U.K. E-mail: peter.scanlon@glos.nhs.uk. Received for publication 9 February 2005 and accepted in revised form 23 June 2005. A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances. © 2005 by the American Diabetes Association. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. P a t h o p h y s i o l o g y / C o m p l i c a t i o n s O R I G I N A L A R T I C L E 2448 DIABETES CARE, VOLUME 28, NUMBER 10, OCTOBER 2005 considered this to be appropriate and was specifically requested to take an anterior segment view of an eye with a poor quality image. Grading Patients for the reference standard ex- amination (n � 1,549) using 78D lens slit-lamp biomicroscopy and direct oph- thalmoscopy were recruited from those attending for photographic screening on days when an experienced ophthalmolo- gist (P.H.S.) was able to attend. A separate study was performed to validate the oph- thalmologist’s reference standard against seven-field stereophotography (18). A specialist registrar in ophthalmol- ogy (R.M.) interpreted the images from the study patients who received the refer- ence standard examination (n � 1,549). P.H.S. interpreted the images of all pa- tients who did not receive his reference standard examination (n � 2,062). Grad- ers had a history sheet, including the pa- tient’s age, diabetes and ophthalmological history, visual acuity, screener’s ophthal- moscopy findings, and reasons for extra views. Nonmydriatic and mydriatic images were graded using Orion software (Cwm- bran, U.K.) with time of grading sepa- rated by at least 1 month to prevent bias from a memory effect. It was not possible to mask the grader between methods be- cause one image of each eye was captured without mydriasis and two images with mydriasis. For grading, 19-inch Sony Tri- nitron monitors were used with a screen resolution of 1,024 � 768 and 32-bit color (although we recognize that the camera system was limited to 24 bit). The Topcon fundus camera with Sony digital camera produced an image of resolution 768 � 568 pixels. Image grading and the reference stan- dard examination used the Gloucester- s h i r e a d a p t a t i o n o f t h e E u r o p e a n Working Party guidelines (19) for refer- able diabetic retinopathy (previously used in the Gloucestershire Diabetic Eye Study [9] and validated against seven- field stereophotography in a separate study [18]), as shown in Table 1. Refer- able retinopathy was classified as grades three to six on this form. The Interna- tional Classification (20) was not used be- cause the current study was undertaken before this was introduced and, even if this was available, referral to an ophthal- mologist in the U.K. is at a level between level 3 and level 4 of the International Classification. The ungradable image rate was clas- sified as the number of patients with an ungradable image in one or both eyes un- less referable diabetic retinopathy was de- tected in either eye. Image quality was judged with reference to each eye on the macular view and an eye was considered ungradable when the large vessels of the temporal arcades were blurred or more than one-third of the picture was blurred unless referable retinopathy was detected in the remainder. The nasal view was re- garded as providing supplementary infor- mation and was not used for image quality assessments. Reexamination of photographs P.H.S. reexamined all the anterior seg- ment photographs from eyes with un- gradable images and any control eyes (i.e., if an anterior segment photograph had been taken of the patient’s other eye) to determine whether cataract was present using the following classifications: 1) ob- vious central cataract: impaired central red reflex with obvious cataract almost certainly contributing to poor image qual- ity; 2) early cataract: some impairment of central red reflex with cataract, which may or may not contribute to poor image quality; and 3) no cataract: good central red reflex and either no cataract or early peripheral lens changes not considered to contribute to poor image quality. The horizontal pupil diameter of all the pupils in the central axis on the 19- inch monitor on which the anterior seg- m e n t i m a g e s w e r e d i s p l a y e d w a s measured. The anterior segment images had been collected using a standardized methodology, so as to maintain near equivalence in image magnification be- tween patients. Any other pathology that might have contributed to impaired qual- ity of retinal images was recorded. Iris color of the ungradable eye was classified as blue, green (including blue with brown flecks or green), light brown, or dark brown. Statistical methods Data were entered into a customized da- tabase in the Medical Data Index (Patient Administration System) at Cheltenham General Hospital and downloaded into SPSS version 10 (SPSS, Chicago, IL) for Table 1 Description Grade right eye Grade left eye Outcome No diabetic retinopathy 0 0 12/12 Minimal nonproliferative diabetic retinopathy 1 1 12/12 Mild nonproliferative diabetic retinopathy 2 2 12/12 Maculopathy 3 3 Refer Hemorrhage �1 DD from foveal center 3a 3a Routine Exudates �1 DD from foveal center 3b 3b Soon Groups of exudates (including circinate and plaque) within the temporal arcades �1 DD from foveal center 3c 3c Soon Reduced VA not corrected by a pinhole likely to be caused by a diabetic macular problem and/or suspected clinically significant macular edema. 3d 3d Soon Moderate to severe nonproliferative diabetic retinopathy 4 4 Refer Multiple cotton wool spots (�5) 4a 4a Soon and/or multiple hemorrhages 4a 4a Soon and/or intraretinal microvascular abnormalities 4b 4b Soon and/or venous irregularities (beading, reduplication, or loops) 4b 4b Soon Proliferative diabetic retinopathy 5 5 Refer New vessels on the disc, new vessels elsewhere, preretinal hemorrhage, and/or fibrous tissue Urgent Advanced diabetic retinopathy 6 6 Refer Vitreous hemorrhage, traction/traction detachment, and/or rubeosis iridis Immediate DD, disc diameter; VA, visual acuity. Scanlon and Associates DIABETES CARE, VOLUME 28, NUMBER 10, OCTOBER 2005 2449 data analysis as required. Percentages and 95% CIs were calculated. Multiple logistic regression was used to assess the impact of more than one predictive factor on the odds of poor image quality. Pupil diameters for ungradable eyes and the opposite gradable eyes (where an- terior segment photographs of both eyes were available) were compared for the un- gradable eyes with no cataract, early cat- aract, and obvious central cataract. To identify any trends, the diameters in un- gradable and opposite eyes and the differ- ence between them were compared between cataract groups using one-way ANOVA with a linear contrast. Age and duration of diabetes were compared be- tween the no cataract and the obvious central cataract group using Mann- Whitney U tests. RESULTS Acceptance rate of screening invitation and nonattendance rate at screening appointment and identification of the study population Of 11,909 people with diabetes in the county, 74% responded to the screening invitation and attended. Of those who re- sponded to the screening invitation and booked an appointment, the attendance rate was 95%. The high response and at- tendance rates enabled the target popula- tion of 3,650 patients from within 80 groups of 50 patients to be identified and examined. Images of 39 patients from one prac- tice were excluded from the study because the patient images were accidentally cap- tured in JPEG format instead of TIFF format. Ungradable image rates were cal- culated for all remaining 3,611 patients in the study. Seven grading forms were absent from the nonmydriatic group, all of which were from the subgroup of 1,549 patients who had the reference standard examination. Ungradable image rate and age The ungradable image rate for nonmydri- atic photography was 19.7% (95% CI 18.4 –21.0) and for mydriatic photogra- phy was 3.7% (3.1– 4.3). A total of 15 patients in the nonmydriatic group and 8 patients in the mydriatic group who were found to have an ungradable image in one eye were not included in the ungradable image rate because referable retinopathy was detected in the other eye (Fig. 1). Detection of referable retinopathy in different age ranges From the reference standard examination of 1,549 patients, 180 patients were found to have referable diabetic retinopa- thy. The grading form for one of these patients (from the nonmydriatic group) was missing, making the maximum pos- sible detection in that group 179. Levels of detection of referable diabetic retinop- athy were 82.8% for mydriatic photogra- p h y ( 1 4 9 o f 1 8 0 ) a n d 5 7 . 5 % f o r nonmydriatic photography (103 of 179). Analyzing the nonmydriatic figures in 10- year age-groups, the younger age-groups had better image quality results and better identification of referable diabetic reti- nopathy (Fig. 2). Type of diabetes, sex of study patients, and duration of diabetes Of 3,611 study patients, 16.5% had type 1 diabetes, 81.6% had type 2 diabetes, and 1.9% had unknown diabetes status. Participants were 55% male and 45% fe- male. Duration of diabetes was 41.7% 0 – 4 years, 26.2% 5–9 years, 13.7% 10 –14 years, 7.6% 15–19 years, 10.8% 20� years, and 0.2% unknown duration. The 1,549 reference standard subgroup patients had very similar characteristics. Ungradable image rate versus age and duration of diabetes Because an association was found be- tween ungradable image rate and both age and duration of diabetes and also between age and duration of diabetes, a logistic re- gression analysis was undertaken to see if Figure 1—Unassessable image patients for mydriatic and nonmydriatic photographic screening. Image quality in diabetic retinal screening 2450 DIABETES CARE, VOLUME 28, NUMBER 10, OCTOBER 2005 the associations were independent of each other. For nonmydriatic photography, the odds of having one eye ungradable in- creased by 2.6% (95% CI 1.6 –3.7) for each extra year since diagnosis, irrespec- tive of age, and by 5.8% (5.0 – 6.7) for every extra year of age, irrespective of years since diagnosis. For mydriatic pho- tography, the odds of having one eye un- gradable increased by 4.1% (2.7–5.7) for each extra year since diagnosis, irrespec- tive of age, and by 8.4% (6.5–10.4) for each extra year of age, irrespective of years since diagnosis. The analysis showed that both age and years since diagnosis con- tributed to the odds of having an ungrad- able image in one eye. Influence of cataract and other pathology Of the 169 ungradable eyes from 133 pa- tients, 8 eyes had no anterior segment im- age. Of the 161 eyes with an anterior segment image, 92 eyes (57%) had obvi- ous central cataract, 34 eyes (21%) had early cataract, and 15 eyes (9%) had no cataract. The study of other pathology showed 10 eyes (6%) had a corneal scar, 9 eyes (6%) had asteroid hyalosis, and 1 eye (1%) had a history of hemorrhage, glau- coma, and blindness (not from diabetic retinopathy). Influence of pupil diameter There were 97 patients in whom one eye was not assessable. In 12 cases, there was a nondiabetic, noncataract pathological reason detected that would explain why imaging was unsuccessful (e.g., corneal scarring), and in 5 cases no anterior seg- ment image was taken of the ungradable eye. In the remaining 80 cases, no obvious other pathology was detected that could explain poor image quality, suggesting a relationship with pupil size. To test this hypothesis, we examined the pupil diam- eter in those 54 cases in which an anterior segment view was available of both the ungradable eye and the gradable fellow eye. The following comparisons were made between the two eyes. In eight eyes with no cataract seen in the ungradable eye, the mean pupil diameter in the un- gradable eye was 2.7 cm and in the grad- able control eye was 3.6 cm (difference: 0.9 cm). In 14 eyes with early cataract seen, the mean pupil diameter in the un- gradable eye was 3.4 cm and in the grad- able control eye was 3.9 cm (difference: 0.5 cm). In 32 eyes with obvious cataract seen, the mean pupil diameter in the un- gradable eye was 4.4 cm and in the grad- able control eye was 4.3 cm (difference: �0.1 cm). The pupil diameter in the un- gradable eye and the difference in pupil diameters between the two eyes both showed significant trends (P � 0.001 and P � 0.008, respectively) in the three groups. However, the pupil diameter in the gradable eye did not show a signifi- cant trend (P � 0.072) in any group. The eight people in the no cataract group with poor pupillary dilation (mean 2.7 cm) had a mean age of 72.7 years and a mean duration of 20.4 years with diabe- tes. The 32 people with obvious central cataract and good pupillary dilation (mean 4.4 cm) had a mean age of 78.5 years and a mean duration of 8.7 years with diabetes. The Mann-Whitney U test showed no significant difference for the ages between these two groups but a sig- nificant difference for duration of diabetes (P � 0.003). Iris color in ungradable eyes Of the 124 patients in whom anterior views enabled color determination, there were 68 blue (55%), 24 green (19%), 21 light brown (17%) and 11 dark brown (9%) eyes. The iris color is in keeping with Gloucestershire’s predominant pro- portional white Caucasian population, the main ethnic minority groups being In- dian/British Indian (0.7%) and Black/ Black British (0.8%). CONCLUSIONS — Several possible factors might have an influence on image quality in retinal photography. Age is sug- gested in the following studies. Higgs et al. (13) reported that 13% �50 years, 39% 50 –70 years, and 54% �70 years had ungradable nonmydriatic images. Buxton et al. (21) reported that the un- gradable image rate varied between 2% in the Exeter physician group and 9% in the Oxford general practitioner group. The difference between these two groups was principally related to age, duration of di- abetes, and type of diabetes. Some studies (3,8) have reported nonmydriatic un- gradable image rates �12%, but the aver- age age of the study population was �55 years. Duration of diabetes is suggested as a factor by Cahill et al. (22), who in 2001 reported that pupillary autonomic dener- vation increases with increasing duration of diabetes mellitus. Ethnicity is sug- gested by Klein et al. (23). Flash intensity is suggested by Taylor et al. (24), who reported less patient dis- comfort with the lower flash power (10 W vs. 300 W) of the digital system. In non- mydriatic photography, there is a faster pupil recovery time with lower flash in- tensities, which may improve image qual- ity in the fellow eye. Age, duration of diabetes, and ethnic- ity were not reported in some studies (7,11,25), while others (1,6) have re- ported these variables but have not re- ported an association. The study by Lin et al. (4) excluded 197 patients (48.5%) for unusable seven-field reference standard photos and a further 12 patients (2.96%) Figure 2—Referable retinopathy by age compared to the reference standard examination. Scanlon and Associates DIABETES CARE, VOLUME 28, NUMBER 10, OCTOBER 2005 2451 because of unusable ophthalmoscopy records, which made it difficult to inter- pret the ungradable image rate of 8.1%. Shiba et al. (5) excluded the �70 years age-group and remarkably attempted 9 � overlapping nonmydriatic 45° fields (5), whereas others have only attempted five fields (8), three fields (2,3), and the ma- jority only one nonmydriatic field (1,6,9,10,13,21). Patient numbers varied from 40 eyes in the study by Lim et al. (2) to 3,611 patients in the current study. The current study has suggested that, after excluding a small number of patients with other pathology, the causes of un- gradable images in mydriatic photogra- phy are obvious central cataract (57%), a combination of early cataract and a small pupil (21%), and a small pupil alone (9%). There was a dip to 75% in the 30 –39 age-group (two patients missed) and 62.5% in the 40 – 49 age-group (six patients missed) in detection of referable retinopathy using mydriatic photogra- phy. If ungradable images were test posi- tive (i.e., referable), six patients in total would have been missed in the 30 – 49 age- group. On retrospective examination of the mydriatic images, the pathology was visible in five of six of these (two hav- ing received extensive laser treatment and being graded as stable treated diabetic ret- inopathy). There was only one person whose retinopathy visible within the two 45° fields was mild nonproliferative dia- betic retinopathy (i.e., not referable), whereas small new vessels elsewhere were visible in the peripheral retina only on ref- erence standard examination. This is the only patient in this age-group that should have been a definite false negative for the test. While a 20% failure rate for nonmyd- riatic photography might be acceptable because patients could be reexamined by other means, there is a difference in de- tection of referable retinopathy between the two methods, as shown in Fig. 2. The Health Technology Board for Scotland used data from the current study in their report (15) and concluded that similar sensitivities and specificities could be achieved by dilating those patients with ungradable images. However, this relies on the ability of the screener to accurately determine an ungradable image at the time of screening and, in the Scottish sys- tem, relies on the assumption that the grading of one field will detect referable retinopathy with the same degree of accu- racy as the grading of two fields (giving evidence from Olson et al.’s study [26]). There have been differing views on the number of fields required for screening, Bresnick et al. (27) supporting Olson et al.’s view that one field may be sufficient. However, studies by Moss et al. (28), Shiba et al. (5), and von Wendt et al. (29) have suggested that higher numbers of fields give greater accuracy in detection of retinopathy levels. Data from the current study indicates that there would potentially be very many occasions on which nonmydriatic imag- ing in patients aged �50 years would re- sult in ungradable images. In the �80 years age-group, the failure rate is re- duced from 41.6 to 16.9% by dilation with G Tropicamide 1%. It is possible that the failure rate of 16.9% following dila- tion with G Tropicamide 1% could be fur- ther reduced by the addition of G Phenylephrine 2.5% for this specific group. Routinely dilating the �50 years age-group with G Tropicamide 1% at out- set could potentially reduce the failure rate by �80%. If screening programs are going to consider nonmydriatic photog- raphy to detect sight-threatening diabetic retinopathy, the findings of the current study largely support the use of this method for the group �50 years of age who are at lowest risk of ungradable im- ages, and yet, this group contains a num- ber of young regular nonattendees, who some authors suggest are at greatest risk of blindness (e.g., MacCuish et al. [30] and Jones [31]). Acknowledgments — This study was funded by the Project Grant South West R&D Direc- torate. P.H.S is submitting this work for an MD thesis to University College London. The study was designed by P.H.S. with the support of C.F, and the article was written by P.H.S. with the help of S.J.A. P.H.S. performed all the clinical examinations, and P.H.S. and R.M. graded all the images. C.F. undertook the data analysis. All coauthors commented on the drafts and helped to interpret the findings. P.H.S. is the guarantor for this publication. References 1. Pugh JA, Jacobson JM, Van Heuven WA, Watters JA, Tuley MR, Lairson DR, Lori- mor RJ, Kapadia AS, Velez R: Screening for diabetic retinopathy: the wide-angle retinal camera. Diabetes Care 16:889 – 895, 1993 2. Lim JI, LaBree L, Nichols T, Cardenas I: A comparison of digital nonmydriatic fun- dus imaging with standard 35-millimeter slides for diabetic retinopathy. Ophthal- mology 107:866 – 870, 2000 3. Bursell SE, Cavallerano JD, Cavallerano AA, Clermont AC, Birkmire-Peters D, Ai- ello LP, Aiello LM, Joslin Vision Network Research Team: Stereo nonmydriatic dig- ital-video color retinal imaging compared with Early Treatment Diabetic Retinopa- thy Study seven standard field 35-mm ste- reo color photos for determining level of diabetic retinopathy. Ophthalmology 108: 572–585, 2001 4. Lin DY, Blumenkranz MS, Brothers RJ, Grosvenor DM: The sensitivity and spec- ificity of single-field nonmydriatic mono- chromatic digital fundus photography with remote image interpretation for dia- betic retinopathy screening: a comparison with ophthalmoscopy and standardized mydriatic color photography. Am J Oph- thalmol 134:204 –213, 2002 5. Shiba T, Yamamoto T, Seki U, Utsugi N, Fujita K, Sato Y, Terada H, Sekihara H, Hagura R: Screening and follow-up of di- abetic retinopathy using a new mosaic 9-field fundus photography system. Dia- betes Res Clin Pract 55:49 –59, 2002 6. Harper CA, Livingston PM, Wood C, Jin C, Lee SJ, Keeffe JE, McCarty CA, Taylor HR: Screening for diabetic retinopathy us- ing a non-mydriatic retinal camera in ru- ral Victoria. Aust N Z J Ophthalmol 26: 117–121, 1998 7. Yogesan K, Constable IJ, Barry CJ, Eikel- boom RH, McAllister IL, Tay-Kearney ML: Telemedicine screening of diabetic retinopathy using a hand-held fundus camera. Telemed J 6:219 –223, 2000 8. Massin P, Erginay A, Ben Mehidi A, Vicaut E, Quentel G, Victor Z, Marre M, Guil- lausseau PJ, Gaudric A: Evaluation of a new non-mydriatic digital camera for de- tection of diabetic retinopathy. Diabet Med 20:635– 641, 2003 9. Scanlon PH, Malhotra R, Thomas G, Foy C, Kirkpatrick JN, Lewis-Barned N, Har- ney B, Aldington SJ: The effectiveness of screening for diabetic retinopathy by dig- ital imaging photography and technician ophthalmoscopy. Diabet Med 20:467– 474, 2003 10. Leese GP, Ahmed S, Newton RW, Jung RT, Ellingford A, Baines P, Roxburgh S, Coleiro J: Use of mobile screening unit for diabetic retinopathy in rural and urban areas. BMJ 306:187–189, 1993 11. Jones D, Dolben J, Owens DR, Vora JP, Young S, Creagh FM: Non-mydriatic Po- laroid photography in screening for dia- betic retinopathy: evaluation in a clinical setting. Br Med J (Clin Res Ed) 296:1029 – 1030, 1988 12. Murgatroyd H, Ellingford A, Cox A, Bin- nie M, Ellis JD, MacEwen CJ, Leese GP: Effect of mydriasis and different field strategies on digital image screening of di- abetic eye disease. Br J Ophthalmol 88: 920 –924, 2004 13. Higgs ER, Harney BA, Kelleher A, Reck- Image quality in diabetic retinal screening 2452 DIABETES CARE, VOLUME 28, NUMBER 10, OCTOBER 2005 less JP: Detection of diabetic retinopathy in the community using a non-mydriatic camera. Diabet Med 8:551–555, 1991 14. Gillow JT, Gray JA: The National Screen- ing Committee review of diabetic retinop- athy screening. Eye 15:1–2, 2001 15. Facey K, Cummins E, Macpherson K, Morris A, Reay L, Slattery J: Organisation of Services for Diabetic Retinopathy Screen- ing. Glasgow, Scotland, Health Technol- ogy Board for Scotland, 2002, p. 1–224 16. Ferris FL, 3rd, Kassoff A, Bresnick GH, Bailey I: New visual acuity charts for clin- ical research. Am J Ophthalmol 94:91–96, 1982 17. Aldington SJ, Kohner EM, Meuer S, Klein R, Sjolie AK: Methodology for retinal photography and assessment of diabetic retinopathy: the EURODIAB IDDM com- plications study. Diabetologia 38:437– 444, 1995 18. Scanlon PH, Malhotra R, Greenwood RH, Aldington SJ, Foy C, Flatman M, Downes S: Comparison of two reference standards in validating two field mydriatic digital photography as a method of screening for diabetic retinopathy. Br J Ophthalmol 87: 1258 –1263, 2003 19. Retinopathy Working Party: A protocol for screening for diabetic retinopathy in Europe. Diabet Med 8:263–267, 1991 20. Wilkinson CP, Ferris FL 3rd, Klein RE, Lee PP, Agardh CD, Davis M, Dills D, Kam- pik A, Pararajasegaram R, Verdaguer JT, the Global Diabetic Retinopathy Project Group: Proposed international clinical di- abetic retinopathy and diabetic macular edema disease severity scales. Ophthal- mology 110:1677–1682, 2003 21. Buxton MJ, Sculpher MJ, Ferguson BA, Humphreys JE, Altman JF, Spiegelhalter DJ, Kirby AJ, Jacob JS, Bacon H, Dud- bridge SB, et al.: Screening for treatable diabetic retinopathy: a comparison of dif- ferent methods. Diabet Med 8:371–377, 1991 22. Cahill M, Eustace P, de Jesus V: Pupillary autonomic denervation with increasing duration of diabetes mellitus. Br J Oph- thalmol 85:1225–1230, 2001 23. Klein R, Klein BE, Neider MW, Hubbard LD, Meuer SM, Brothers RJ: Diabetic retinopathy as detected using ophthal- moscopy, a nonmydriatic camera and a standard fundus camera. Ophthalmology 92:485– 491, 1985 24. Taylor DJ, Fisher J, Jacob J, Tooke JE: The use of digital cameras in a mobile retinal screening environment. Diabet Med 16: 680 – 686, 1999 25. Williams R, Nussey S, Humphry R, Thomp- son G: Assessment of non-mydriatic fun- dus photography in detection of diabetic retinopathy. Br Med J (Clin Res Ed) 293: 1140 –1142, 1986 26. Olson JA, Strachan FM, Hipwell JH, Goat- man KA, McHardy KC, Forrester JV, Sharp PF: A comparative evaluation of digital imaging, retinal photography and optometrist examination in screening for diabetic retinopathy. Diabet Med 20:528 – 534, 2003 27. Bresnick GH, Mukamel DB, Dickinson JC, Cole DR: A screening approach to the surveillance of patients with diabetes for the presence of vision-threatening reti- nopathy. Ophthalmology 107:19 –24, 2000 28. Moss SE, Meuer SM, Klein R, Hubbard LD, Brothers RJ, Klein BE: Are seven stan- dard photographic fields necessary for classification of diabetic retinopathy? In- vest Ophthalmol Vis Sci 30:823– 828, 1989 29. von Wendt G, Heikkila K, Summanen P: Detection of retinal neovascularizations using 45 degrees and 60 degrees photo- graphic fields with varying 45 degrees fields simulated on a 60 degrees photo- graph. Acta Ophthalmol Scand 80:372– 378, 2002 30. MacCuish AC: Early detection and screening for diabetic retinopathy. Eye 7:254 –259, 1993 31. Jones RB, Larizgoitia I, Casado L, Barrie T: How effective is the referral chain for di- abetic retinopathy? Diabet Med 6:262– 266, 1989 Scanlon and Associates DIABETES CARE, VOLUME 28, NUMBER 10, OCTOBER 2005 2453