Optic Disc Cupping: Four Year Follow-up from the WESDR

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1 Investigative Ophthalmology & Visual Science, Vol. 30, o., February 989 Copyright Association for Research in Vision and Ophthalmology Optic Disc Cupping: Four Year Follow-up from the WER Barbara E. K. Klein, Scot E. Moss, Yvonne L. Mogli, Ronald Klein, Carol Hoyer, and Judyrh Johnson Change in optic disc cupping was evaluated in a 4-year follow-up of a well defined cohort of people with diabetes mellitus. Cup-to-disc ratios were computed for both vertical and horizontal diameters of each eye at the baseline and 4-year follow-up examinations. Graders were masked as to the identity of participants and to the dates of the photographs. Increases of at least 0. between baseline and follow-up were used as clinically significant change in the ratios. one of the following factors at baseline were consistent predictors of such a change: intraocular pressure, age, duration of diabetes, hypertension or severity of diabetic retinopathy. People who developed proliferative retinopathy by the follow-up examination were not more likely to have such an increase in ratio at the follow-up. We conclude that clinically significant increases in cup-to-disc ratio cannot be consistently predicted in people with diabetes from the risk factors evaluated with the grading system used in this study. Invest Ophthalmol Vis Sci 30:30-35,989 The ratios of the diameters of the optic cup to the disc are anatomic parameters, the dimensions of which may be determined by heredity. However, clinical experience indicates that the diameter of the cup can be altered by pathologic conditions. Thus, the cup can appear smaller if there is obscuration due to new blood vessel or fibrous tissue growth on the disc; it can actually be smaller if there is swelling of the nerve fibers surrounding the cup as would occur with papilledema, or diabetic papillopathy or possibly with optic disc drusen. " 4 The cup can enlarge in those conditions that cause destruction of the nerve fibers such as occurs in glaucoma, and also possibly when there has been atrophy due to vascular compromise or optic nerve atrophy. Because people with diabetes have been thought to be at increased risk of glaucoma 5 ' 6 and also because of the possibility of ischemia during the course of diabetic retinopathy and its treatment, one might anticipate an average increase in the cup-to-disc ratio during an interval of several years of diabetes. We had the opportunity to investigate this question in data from the cohort of diabetic persons in the Wisconsin Epidemiologic From the Department of Ophthalmology, University of Wisconsin Medical School, Madison, Wisconsin. Supported by ational Institutes of Health Grants EY (BEKK) and EY (RK). Submitted for publication: May 6, 988; accepted September, 988. Reprint requests: B. E. K. Klein, MD, MPH, Department of Ophthalmology, University of Wisconsin, 600 Highland Avenue, Madison, WI Study of Diabetic Retinopathy (WER) who were seen in and again in Materials and Methods Population The population has been described in detail in previous reports. 7 " 9 Briefly, a population-based sample of 990 diabetic persons was selected for the first examination of the Wisconsin Epidemiologic Study of Diabetic Retinopathy. Of these, 366 participated in the first examination during During the follow-up examination in , 79.4% of this cohort was reexamined. 0 '" The most frequent cause of nonparticipation in the second examination was death (n = 404); only 46 people refused to participate in the follow-up examination. Further description of the nonparticipants in the follow-up are described elsewhere. l0 ~ Informed consent was obtained from each participating subject. Procedures Baseline and follow-up examinations were performed in a mobile examination van in or near the city where the participants resided. All procedures were performed according to standard protocols and included measuring blood pressure, 3 intraocular pressure, 4 best corrected visual acuity," performing a slit lamp examination, dilating the pupils, taking stereoscopic color photographs of the optic fundus of each eye, and determining glycosylated hemoglobin. 6 Standardized interviews were conducted at 30

2 o. CHAGE I DISC CUPPIG I DIABETES / Klein er al 3 Table. cup-to-disc ratios of right eyes from baseline and follow-up photographs Baseline Follow-up Baseline Follow-up p* p* Based on a paired t-test. each examination during which the participant was asked whether he/she had ever been told that he/she had glaucoma or were on medication for glaucoma. This historical information was used when classifying people as to presence or absence of a history of glau- Cup and Disc Diameter Measurements Details of the grading scheme have been published elsewhere. 7 Briefly, stereoscopic photographs of the optic discs were measured in the vertical and horizontal dimensions according to a standard protocol using a measuring template. Each eye was graded independently by two graders, and differences were adjudicated by a senior grader. The mean of the two graders was used as the final measurement for each eye. Severity of Diabetic Retinopathy Stereoscopic fundus photographs of each eye were taken of seven standard fields and were graded using a modification of the Airlie House Classification Scheme. 8 The severity of diabetic retinopathy was classified according to the following scheme: level represents no diabetic retinopathy; levels.5 to 5 represent increasing severity of nonproliferative retinopathy; level 6 indicates fibroproliferans only or early proliferative retinopathy; level 7 represents proliferative retinopathy with Diabetic Retinopathy Study High Risk Characteristics for severe visual loss 9 and level 8 represents the most severe retinopathy such that the eyes were ungradable due to vitreous hemorrhage or other complications of diabetic retinopathy. Definitions Current age and duration were as ascertained at the baseline examination. Data Handling and Analysis Wisconsin Storage and Retrieval, an information processing software system, was used for processing all subject files. Statistical Analysis System was used for calculating the student t-test, analysis of variance, and multiple linear regression. Results cup-to-disc ratios are given in Table for baseline and follow-up measurements. Differences in ratios between baseline and follow-up were not significant. There were no systematic differences between right and left eyes. Because of inherent variability in the measurement technique and because change in cup-to-disc ratio of less than 0. is clinically difficult to judge, we performed the following analyses of relationships of possible risk factors to change in cupping to those cases in which the increase was at least 0. and confined our descriptions to right eyes. Cup-todisc ratios were not more likely to increase than to decrease at least this much at the follow-up exam. Table. Frequency of change in cup-to-disc ratios of the right eye at follow-up for older onset patients by glaucoma status ratio at follow-up minus vertical ratio at baseline &0. ratio at follow-up minus horizontal ratio at baseline 0. o glaucoma Glaucoma 8/374 0/0 7/370 0/9 o glaucoma Glaucoma /334 /6 8/39 0/6

3 3 IVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIECE / February 989 Vol. 30 Table 3. Increase in cup/disc ratios S; 0. in the right eye by IOP at baseline Youni%er onset IOP < a 0/7 0/3 /55 6/74 4/74 /67 4/4 / /7,. 0/3 /54 5/74 3/73 /64 /4 3/ /8 0/ /46 0/67 3/79 /60 3/37 3/3 <0.0i 0/8 0/ /44 /66 3/78 0/59 0/37 / /0 0/5 /9 4/5 8/53 4/4 8/96 /37 <0.05 0/0 /5 3/9 4/47 4/5 3/4 4/95 / * Based on logistic regression. With regard to possible risk factors for increased cupping, the first factor evaluated was a past history of glaucoma. There were too few cases in the younger onset group who had been seen at both examinations to evaluate this. In older onset persons an increase in ratio of at least 0. was infrequent in those with and without a history of glaucoma and there was no significant increase associated with a history of glaucoma (Table ). In order to determine whether intraocular pressure was positively associated with increased cupping, we computed the change in cupping between the two visits by IOP at baseline exam. There were significant changes in the vertical ratios of the right eye in the older onset insulin users and younger onset groups (Table 3). In like manner, we computed the change in ratios with increasing age (Table 4), and with increasing duration of diabetes (Table 5) at the baseline exam. There was no significant increase in ratios with age or duration for any group. Because greater severity of diabetic retinopathy was considered to be a possible risk factor for increased cupping, we calculated the change in cupping for each level of severity of diabetic retinopathy (Table 6); people who had had panretinal photocoagulation at baseline were evaluated as a separate severity group. There was no effect of increasing severity of diabetic retinopathy and subsequent increased ratios in any group. High blood pressure has been related in some studies to the presence of glaucoma. To evaluate the possible effect of high blood pressure (systolic blood pressure > 60 and/or diastolic blood pressure > 95) as a predictor of increased cupping, we computed the change in cupping over the interval by blood pressure status at the baseline exam. For neither vertical nor horizontal ratio for any of the three groups was there a significant change (Table 7). There was no evidence of an effect of high blood pressure that had been successfully treated (blood pressure less than cutpoints above) during the interval on increased cupping in either diameter in any group (data not presented). In order to determine whether changes in retinopathy during the time between exams affected the ratios, we calculated change in the cup-to-disc ratios for people in whom proliferative retinopathy developed in the interval. There was no evidence of increased cupping in those with proliferative retinopathy compared to those who did not progress to proliferative retinopathy in any group for either diameter (Table 8). There were too few people who had received laser treatment in the 4-year interval to evaluate a possible relationship of such treatment to change in optic disc cupping. Multiple linear regression analysis was performed Table 4. Increase in cup/disc ratios s; 0. in the right eye by age at baseline Older onset. no insulin Yountyer onset Age Age s75 /9 3/47 5/3 8/36 0/5 0/8 5/46 6/3 4/35 / / 4/75 3/5 4/07 / / 4/74 /5 /05 / &45 0/9 5/6 5/33 6/ / /9 /6 /3 7/6 / ' Based on logistic regression.

4 o. CHAGE I DISC CUPPIG I DIADETES / Klein er ol 33 Table 5. Increase in cup/disc ratios ^ 0. by duration of diabetes at baseline Duration ;>30 0/6 6/6 /37 /4 0/ 0/6t /59 3/6 /37 /39 / 0/6t 0.9 3/6 /6 /6 /87 / /9 /0 0.4 /6 /59 /60 /85 0/5 /9 / /4 5/ 6/33 4/93 6/60 /46 0/ /40 4/ 4/3 6/89 /60 3/45 0/ 0.58 * Based on logistic regression. f For duration ^5. to determine whether several variables would be significant descriptors of an increase in optic disc cupping. The following characteristics at the baseline exam were included as independent variables in all models: severity level of diabetic retinopathy, intraocular pressure, age, duration of diabetes, percent glycosylated hemoglobin, systolic blood pressure, diastolic blood pressure, use of diuretic medications, proteinuria, sex, and history of glaucoma. There was no association in any model between the independent variables and increased vertical or horizontal cup-todisc ratio. Discussion Optic disc cupping is often used clinically as a parameter to follow when trying to assess the effects of intraocular pressure. One would anticipate that such an effect would be more likely to occur in the presence of ocular tissues that may be compromised by another condition. In the current study comprised of people with diabetes, many with retinopathy, such an effect was not apparent over a four year follow-up. If such an effect is real, it may be that four years is too short an interval to detect it. One might speculate as to why a history of glaucoma did not predispose to increased cupping. It may be that since glaucoma in diabetic persons is a risk indicator for subsequent death, people who would have had increased cupping died before the follow-up exam or were too ill to participate. Another possibility is that using a history of glaucoma for case definition leaves many undiagnosed cases in the "no glau- Table 6. Change in cup/disc ratio, OD between baseline and follow-up by the severity of diabetic retinopathy for persons without panretinal photocoagulation Group Severity of diabetic retinopathy Older onset, no insulin Older onset, insulin PDR PDR PDR

5 34 IVESTIGATIVE OPHTHALMOLOGY & VI5UAL SCIECE / Februory 989 Vol. 30 Table 7. Increase in cup/disc ratio ^ 0. in the right eye by blood pressure status at baseline Blood pressure High ormal /43 5/ /43 3/ /3 0/66 /3 6/ /43 4/670 /43 8/ Based on Fisher's exact test. Table 8. Increase in cup/disc ratios S: 0. in the right eye by development of proliferative retinopathy at follow-up Retinopathy at follow-up on-proliferative Proliferative 8/376 0/4 7/37 0/4 0/3 0/5 6/306 0/5 /599 3/ /596 3/6 0.3 ' Based on Fisher's exact test. coma" group. This would diminish the difference between glaucoma cases and non-cases. This is not likely to have much effect on the significance test as the number of undiagnosed cases is likely to be small compared to the total number of true non-cases. We did not find increased cupping in people with hypertension at baseline nor did we find a relationship between successfully treated hypertension and increased cupping. This is not consistent with findings of Leske et al who found an effect of hypertension on glaucoma. It may be that blood pressure is not directly related to optic disc cupping or that an effect is not readily demonstrated except when an acute dramatic fall in blood pressure occurs. The method of measurement of cup-to-disc ratio has been shown to be reproducible. 7 There is, of course, inherent variability in the technique. Perhaps a mechanical scanner with the ability to estimate volume of the optic cup would show some effect of the combination of variables that we assessed on cupping. However, the changes found would be subtle indeed and possibly of limited use to a clinician who must judge cupping in a clinical setting. 3 We conclude that in diabetic persons, increases in optic disc cupping cannot be reliably predicted using common ophthalmic parameters with the grading system used in this Study. Key words: change in cupping, diabetes, epidemiology, intraocular pressure Acknowledgments The authors wish to thank Judyth Johnson for grading optic discs, Stacy M. Meuer for photograph and data management, and Mae Wildt for manuscript preparation. References. Farber MD, Klein BEK, and Klein R: Quantification of macular drusen, cup/disc ratios, and intraocular pressures in 36 pairs of monozygotic and 7 pairs of dizygotic twins. ARVO Abstracts. Invest Ophthalmol Vis Sci 9(Suppl):, Tso MOM: Pathology and pathogenesis of drvisen of the optic nervehead. Ophthalmology 88:066, Spencer WH: Drusen of the optic disc and aberrent axoplasmic transport. Am J Ophthalmol 85:, Spencer WH: In Discussion of Tso, MOM: Pathology and pathogenesis of drusen of the optic nervehead. Ophthalmology 88:079, Armstrong JR, Daily RK, Dobson HL, and Girard LJ: The incidence of glaucoma in diabetes mellitus. Am J Ophthalmol :55, Becker B: Diabetes mellitus and primary open-angle glaucoma. Am J Ophthalmol 7:, Klein R, Klein BEK, Syrjala SE, Davis MD, Meuer MM, and Magli Y: The Wisconsin Epidemiologic Study of Diabetic Retinopathy: I. Relationship of diabetic retinopathy to management of diabetes: Preliminary report. In Diabetic, Renal- Retinal Syndrome, Friedman EA and L'Esperance FA, editors. ew York, Grune and Stratton, 98, pp Klein R, Klein BEK, Moss SE, Davis MD, and DeMets DL: II. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol 0:5, Klein R, Klein BEK, Moss SE, Davisv rfd, and DeMets DL: III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol 0:57, Klein R, Klein BEK, Moss SE, Davis MD, and DeMets DL: IX. Four-year incidence and progression of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol, in press.. Klein R, Klein BEK, Moss SE, Davis MD, and DeMets DL: X. Four-year incidence and progression of diabetic retinopathy

6 o. CHAGE I DISC CUPPIG I DIABETES / Klein er a I 35 when age at diagnosis is 30 years or more. Arch Ophthalmol, in press.. Klein R, Moss SE, Klein BEK, and DeMets DL: The relation of ocular and systemic factors to survival in diabetes. Arch Int Med, in press. 3. Hypertension Detection and Follow-up Program Cooperative Group: The hypertension detection and follow-up program. Prev Med 5:7, Klein BEK, Klein R, and Moss SE: Intraocular pressure in diabetic persons. Ophthalmology 9:356, Early Treatment Diabetic Retinopathy Study: Manual of Operations, Baltimore, Early Treatment Diabetic Retinopathy Study Coordinating Center, Department of Epidemiology and Preventive Medicine, University of Maryland, 985; Chapter. U.S. Department of Commerce. ational Technical Information Service, 585 Port Royal Road, Springfield, Virginia, 6, Accession #PB853006/AS. 6. Isolab (Akron, OH) Quik-Step, Fast Hemoglobin Test System. -8, Klein BEK, Magli YL, Richie KA, Moss SE, Meuer SM, and Klein R: Quantitation of optic disc cupping. Ophthalmology 9:654, Diabetic Retinopathy Study Research Group: Report 7: A modification of the Airlie House Classification of diabetic retinopathy. Invest Ophthalmol Vis Sci :, Diabetic Retinopathy Study Research Group: Report #8: Phctocoagulation treatment of proliferative diabetic retinopathy: Clinical application of Diabetic Retinopathy Study findings. Ophthalmology 88:583, 98.. Entine S, Holladay D, and Oschesky T: WISAR: Wisconsin Storage and Retrieval System. University of Wisconsin-Madison, Clinical Cancer Center, 98.. SAS Institute, Inc.: SAS User's Guide: Statistics, Version 5, ed. Cary, orth Carolina, SAS Institute, Inc, 985. p Leske MC, Warheit-Roberts L: Risk factors for open-angle glaucoma. ARVO Abstracts. Invest Ophthalmol Vis Sci 7(Suppl):44, Klein BEK, Moss SE, Magli YL, Klein R, Johnson JC, and Roth H: Optic disc cupping as clinically estimated from photographs. Ophthalmology 94:48, 987.

Optic Disc Cupping: Prevalence Findings from the WESDR

Investigative Ophthalmology & Visual Science, Vol., o. 2, February 1989 Copyright Association for Research in Vision and Ophthalmology Optic Disc Cupping: Prevalence Findings from the WER Barbara E. K.