E p i d e m i o I o g y / H e a 11 h S e r v i c e s / P s y c h o s o c i a I

N A L A R T I C L E

Research

The Prevalence of Diabetic Retinopathy and Associated Risk Factors Among Sioux Indians
DANIEL M. BERINSTEIN, MD GARY R. LEONARDSON, PHD J O H N J . HERLIHY, MD

RESEARCH DESIGN AND

M E T H O D S All diabetic SHS participant members of the Cheyenne River Sioux Tribe and the Oglala Sioux Tribe were invited to take part in this study. The SI IS is a project funded by National Heart, Lung, and Blood Institute to study cardiovascular diseases and associated risk factors in the American Indian communities of North and South Dakota, Oklahoma, and Arizona. Prevalence rates for diabetes among SHS participants aged 45-75 years in North and South Dakota are 33% for men and 46% for women (5). All members of the participating tribes aged 45-74 years were invited to undergo a standardized physical examination and laboratory and diagnostic testing and to answer questionnaires regarding lifestyle and medical history (6,7). In North and South Dakota, 5 1 % of eligible women and 59% of eligible men participated in the study. There was no statistically significant difference in the self-reported prevalence of diabetes among the participants and randomly selected nonparticipants. SHS participants were diagnosed with diabetes by a glucose challenge test (75 g) with a 2-h postchallenge level > 2 0 0 mg/dl. Participants who were already told by a medical care provider that they had diabetes and were being treated with either insulin or oral hypoglycemic medications were considered to have diabetes and were not given a glucose challenge test. SHS participants who consented to participate in this study had a complete eye examination, testing visual acuity, intraocular pressure, and slit-lamp evaluation at local field clinics at their respective reservations. The pupils were dilated and fundus photographs were obtained of each eye with a Topcon nonmydriatic camera using 3 5-mm slide film. Both the macula and superior temporal retinal fields were photographed for each eye, yielding a total of four photos for each patient (two for each eye). The photos were evaluated and graded by a local consultant ophthalmologist (JJ-H.) trained in vitreoretinal diseases for diagnostic and treatment recommendations. All participants with retinopathy were informed through their respective clinics and offered

RUGGLES M. STAHN, MD, MPH

THOMAS K. WELTY, MD, MPH

OBJECTIVE To estimate the prevalence of and risk factors for diabetic retinopathy among Sioux Indians of South Dakota. RESEARCH DESIGN A N D METHODS Strong Heart Study (SHS) participants with diabetes who are members of the Cheyenne River Sioux Tribe and the Oglala Sioux Tribe were invited to have ophthalmological examinations in 1991. A total of 417 people had eye examinations out of the 488 diabetic SHS participants of the two tribes (85% participation rate). Fundus photographs were obtained of each eye and graded for severity of retinopathy using the modified Airlie House Classification Scheme. Risk factors for retinopathy were determined from the SHS database. RESULTS The prevalence of diabetic retinopathy among participants from these tribes was 45.3%. Risk factors associated with severity of retinopathy include mean fasting glucose level, HbAlc, systolic blood pressure, urinary albumin-to-creatinine ratio, renal dialysis, and duration of diabetes. CONCLUSIONS The prevalence of diabetic retinopathy among diabetic Sioux Indians is similar to or higher than the prevalence in other diabetic Indian and non-Indian populations. Aggressive glycemic and blood pressure control is urgently needed to reduce this high rate, and annual eye examinations to detect and treat diabetic retinopathy should be emphasized.

iabetes is a major health concern among the Northern Plains Indians. Since the 1940s, the prevalence of NIDDM has progressively increased to epidemic proportions (1). The Aberdeen Area of the Indian Health Services (IHS) comprises 17 tribes located on 15 service units in North and South Dakota, Nebraska, and Iowa. Its age-adjusted prevalence rate for diagnosed diabetes of 105.4 per 1,000 is the second highest for all areas in the IHS and is 1.5 and 4.2 times higher than the overall IHS and U.S. rates, respectively (2). The Northern

Plains Indians, primarily the Sioux, have an age-adjusted prevalence rate of 92.4 per 1,000, which is 3.7 times the U.S. rate (3). Diabetes is the leading cause of new cases of blindness in people 20-74 years old in the U.S., with ~ 4 - 6 million people with diabetes having retinopathy (4). In this study, we estimate the prevalence of diabetic retinopathy among Sioux Indians participating in the Strong Heart Study (SHS). Additionally, risk factors are identified and compared with other diabetic Indian populations.

From the New York Medical College (D.M.B.), Valhalla, New York; the Aberdeen Area Indian Health Service (R.M.S., T.K.W, G.R.L.), Public Health Service Indian Hospital; the Office of Educational Research (J J.H.); and the Department of Ophthalmology, University of South Dakota School of Medicine, Rapid City, South Dakota. Address correspondence and reprint requests to Thomas K. Welty, MD, MPH, Aberdeen Area Indian Health Service, Department of Epidemiology, 3200 Canyon Rd., Rapid City, SD 57702. Received for publication 25 July 1996 and accepted in revised form 22 November 1996. dBP, diastolic blood pressure; IHS, Indian Health Services; NPR, nonproliferative retinopathy; PDR, proliferative diabetic retinopathy; sBP, systolic blood pressure; SHS, Strong Heart Study; UACR, urinary albumin-to-creatinine ratio.

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Diabetic retinopathy among Sioux Indians

Table 1Presence of diabetic retinopathy Percentage No retinopathy NPR PDR Total 226 166 21 413 54.7 40.2 5.1 100

the categorical variables of renal dialysis (yes or no) and level of retinopathy (no retinopathy, NPR, PDR). For renal dialysis analysis, the no retinopathy and NPR categories were combined into one group. P values of <0.05 were considered to be statistically significant. The protocol for this study was reviewed and approved by the Aberdeen Area and Indian Health Service institutional review boards and by the Cheyenne River Sioux Tribe and the Oglala Sioux Tribe. RESULTS A total of 417 people had eye examinations out of the 488 diabetic SHS participants of the two tribes (85% participation rate). Information on at least one eye was available for only 413 people. Approximately 45.3% of the peoples eyes whose photos were evaluated had diabetic retinopathy, with 40.2 and 5.1% having NPR and PDR, respectively (Table 1). Five factors were identified as being associated with severity of retinopathy (P < 0.001) (Table 2). The mean fasting glucose level was 201 and 210 mg/dl in participants with NPR and PDR, respectively This was significantly higher than 174 mg/dl in participants with no retinopathy. The mean HbA lc level, a measure of glycemic control over the past 2-3 months, was 9.3% in PDR vs. 7.7% and 8.9% in participants with no retinopathy and NPR, respectively. The mean sBP in participants with PDR was 143 mmHg, 131 mmHg for NPR, and 124 mmHg for no retinopathy The UACR was 1,807 in participants with PDR, 560 for NPR, and 53.1 for no retinopathy The average duration of diabetes in participants with NPR was 12.3 years, as compared with 14.2 years for participants with PDR. Significantly more participants with PDR were receiving renal dialysis than participants with no retinopathy or NPR (12 vs. 1%; P = 0.01). We found age, sex, dBP, years of smoking, alcohol history (drinks per day and drinks per week), stroke, physical activity, blood cholesterol, and BMI were not significantly associated with retinopathy in

this population. This may be due to the small sample size and/or characteristics of this population. C O N C L U S I O N S The prevalence of diabetic retinopathy among this group of diabetic Sioux Indians was 45.3%. Rates reported in studies of other U.S. (9-12) and U.S. Indian diabetic populations (13-15) are summarized in Table 3. Fasting blood glucose, HbA lc , sBP, renal disease, dialysis, and duration of diabetes were significantly associated with the severity of retinopathy. West et al. (13) reported a prevalence rate of diabetic retinopathy in Oklahoma Indians to be 24.4% and found duration of diabetes, plasma triglyceride level, and fasting plasma glucose level to be significantly associated with the severity of retinopathy. We identified similar risk factors; however, triglyceride levels were not evaluated in our study Another study among Oklahoma Indians (Cheyenne-Arapaho) reported prevalence rates of diabetic retinopathy to be 49.3% (14). Factors associated with a higher prevalence of retinopathy included sBP, duration of diabetes, history of heart attack, history of stroke, and renal disease. We did not find history of stroke to be a significant factor. Our assessment of stroke was based on patient history and/or clinic charts; therefore, it could be underestimated. The prevalence of diabetic retinopathy in Pima Indians was reported to be 18% (15). Factors shown to have a relationship to the degree of retinopathy were plasma glucose level and duration of diabetes. Age was found not to be a risk factor. Although the Pima prevalence rate was lower, risk factors were similar to our findings among the Sioux Indians. The methods in defining the severity of retinopathy in the other Indian population studies did not use the modified Airlie House classification scheme. However, prevalence studies in the Hispanic population of San Luis Valley using this classification scheme are comparable (12). Our

appropriate treatment. The photos were further evaluated and graded by the University of Wisconsin-Madison School of Medicine Department of Ophthalmology, using the modified Airlie House Classification Scheme (8). All readable photos were graded as follows: no retinopathy, nonproliferative retinopathy (NPR; hard exudates, soft exudates, intravascular microvascular abnormalities without microaneurysms, retinal hemorrhage without microaneurysms, or microaneurysms only), proliferative diabetic retinopathy (PDR), or nondiabetic retinopathy. Photos deemed ungradable as either having no retinal detail, poor field definition, or poor photo quality from decreased clarity or media opacity were excluded from the study. Risk factors were evaluated by comparing the graded level of retinopathy with data from the SHS that included age, duration of diabetes, fasting glucose, HbA lc , systolic blood pressure (sBP), diastolic blood pressure (dBP), total and HDL cholesterol, urinary albumin-to-creatinine ratio (UACR), renal dialysis, smoking and alcohol history, history of stroke, exercise, and BMI. Analysis of variance with a modified least-squares comparison procedure was used to test the differences in the mean values of risk factors among participants with no retinopathy, NPR, and PDR. Logistic regression was not used because missing information for some of the important variables resulted in equations with only about 100 cases. Fishers exact probability test was used to examine the relationship between

Table 2Factors associated with retinopathy (P < 0.001) No retinopathy Mean 173.6 7.7 123.6 53.1 6.4 NPR Mean 209.9 8.9 130.6 559.5 12.3 PDR Mean 201 9.3 142.7 1,807 14.2

n Fasting glucose (mg/ml) HbAlc (%) sBP (mmHg) UACR Duration of diabetes (years) 177 170 183 178 118

SD 7.8
2.6

n 120 115 126 120

115

SD 77.3 2.0 20.1 1,259.9 7.5

n 14 14 16 14 16

SD 79.5 2.5 31.1 2,135.8 10.3

17.8 116 7.9

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Table 3Prevalence rates of diabetic retinopathy in NIDDM diabetic populations Population Sioux (South Dakota) Comanches, Kiowas, Cheyenne-Arapaho, Seminoles, Creeks (Oklahoma) (13) Cheyenne-Arapaho (Oklahoma) (14) Pima (Arizona) Hispanic (San Luis Valley, Colorado) (12) San Antonio, Texas (9) South-central Wisconsin (NIDDM only) (11) Number studied Rate (%)

417 142 973 1,640 279 257 1,370

45 24 49 18 42 45 39

7.

8.

protocol of two photographs for each eye and of the use of color photographs alone may underestimate the prevalence of retinopathy in this population. The modified Airlie House classification defines seven standard stereo photographic fields in classifying retinopathy (8). Owing to limited resources and equipment, 14 photographs for each patient were not feasible. The Diabetes Control and Complications Trial Research Group showed that with use of color photographs alone, ~ 2 0 % of patients with no retinopathy had evidence of retinopathy on fluorescein angiogram (16). In conclusion, the estimated prevalence rate of diabetic retinopathy among the Sioux Indians is 45.3%, with fasting blood glucose, HbA lc , sBP, duration of diabetes, and renal disease as being significant risk factors. These results are reflective of the health needs of the Sioux Indian population. By implementing aggressive glycemic and blood pressure control, the prevalence of diabetic retinopathy could be reduced. The high prevalence of retinopathy also stresses the need for annual eye examinations in this population. Such intervention will allow early diagnosis and treatment, thereby preserving vision and preventing blindness.

Department of Ophthalmology for grading the fundus photos; Barbara Howard, PhD.; Richard Fabsitz; Elisa Lee, PhD; Richard Devereux, MD; and Joseph B. Walsh, MD, for their invaluable comments. D.M. Berinstein is currently at The New York Eye and Ear Infirmary, New York, NY; G.R. Leonardson is currently with Mountain Plains Research, Bozeman, Montana; and J.J. Herlihy is currently in private practice, Rapid City, South Dakota. This paper is in honor of Ruggles Stahn, MD, MPH, whose presence is missed by all who worked with him. He died February 18, 1994, in a tragic plane crash in Minot, North Dakota, while serving Indian patients.

9.

10.

11.

Acknowledgments The opinions expressed in this paper are ours and do not necessarily reflect the views of the Indian Health Service. We would like to thank the participants of the study; we are also indebted to all of the health care providers and staff who planned and implemented the eye examinations in the Pine Ridge and Cheyenne River reservations, including the Black Hills Regional Eye Institute; Mary Buurma, PAC, and Joseph Hartford, OD; The University of Wisconsin School of Medicine

12. References 1. Gohdes DM: Diabetes in American Indians: a growing problem. Diabetes Care 9:609-613, 1986 2. Valway S, Freeman W, Kaufman S, Welty T, Helgerson SD, Gohdes D: Prevalence of diagnosed diabetes among American Indi- 13. ans and Alaska Natives, 1987: estimates from a national outpatient data base. Diabetes Care 6 (Suppl. l):271-276, 1993 3. Stahn RM, Gohdes D, Valway SE: Diabetes 14. and its complications among selected tribes in North Dakota, South Dakota, and Nebraska. Diabetes Care 16 (Suppl. l):244-247, 1993 4. Klein R, Klein B: Vision disorders in dia- 15. betes. In Diabetes in America. 2nd ed. Washington, D.C., U.S. Govt. Printing Office, 1995 (NIH publ. no. 95-1468) 5. Lee ET, Howard BV Savage PJ, Cowan LD, Fabsitz RR, Oopik AJ, Yeh JL, Go O, Robbins DC, Welty TK: Diabetes mellitus and impaired glucose tolerance in three Ameri- 16. can Indian populations aged 45-74 years: The Strong Heart Study. Diabetes Care 18:599-610, 1995 6. Lee ET, Welty TK, Fabsitz R, Cowan LD, Le NA, Oopik AJ, Cucchiara AJ, Savage PJ,

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