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N A L A R T I C L E
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.
DIABETES CARE, VOLUME 20, NUMBER 5, MAY 1997
soft exudates. 131 mmHg for NPR. history of stroke. Indian diabetic populations (13-15) are summarized in Table 3. Factors shown to have a relationship to the degree of retinopathy were plasma glucose level and duration of diabetes.1 for no retinopathy The average duration of diabetes in participants with NPR was 12. proliferative diabetic retinopathy (PDR). The mean sBP in participants with PDR was 143 mmHg. smoking and alcohol history.6 559. Information on at least one eye was available for only 413 people. or poor photo quality from decreased clarity or media opacity were excluded from the study. was 9. history of heart attack.7 123. 7.3 PDR Mean 201 9.S. RESULTS — A total of 417 people had eye examinations out of the 488 diabetic SHS participants of the two tribes (85% participation rate). MAY 1997 . years of smoking. Although the Pima prevalence rate was lower. nonproliferative retinopathy (NPR.2 years for participants with PDR. and fasting plasma glucose level to be significantly associated with the severity of retinopathy.8 10. For renal dialysis analysis. P values of <0. HbA lc .S. physical activity. retinal hemorrhage without microaneurysms. The prevalence of diabetic retinopathy in Pima Indians was reported to be 18% (15). and BMI were not significantly associated with retinopathy in this population.001) No retinopathy Mean 173. (13) reported a prevalence rate of diabetic retinopathy in Oklahoma Indians to be 24.6 7. Risk factors were evaluated by comparing the graded level of retinopathy with data from the SHS that included age. The methods in defining the severity of retinopathy in the other Indian population studies did not use the modified Airlie House classification scheme. Factors associated with a higher prevalence of retinopathy included sBP.1% having NPR and PDR. The mean HbA lc level. hard exudates. duration of diabetes. We did not find history of stroke to be a significant factor. 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. and BMI.7 1. NUMBER 5.3% (14). urinary albumin-to-creatinine ratio (UACR). The photos were further evaluated and graded by the University of Wisconsin-Madison School of Medicine Department of Ophthalmology. a measure of glycemic control over the past 2-3 months. Significantly more participants with PDR were receiving renal dialysis than participants with no retinopathy or NPR (12 vs.2 n Fasting glucose (mg/ml) HbAlc (%) sBP (mmHg) UACR Duration of diabetes (years) 177 170 183 178 118 SD 7. or nondiabetic retinopathy. alcohol history (drinks per day and drinks per week). respectively (Table 1). renal dialysis. and duration of diabetes were significantly associated with the severity of retinopathy.6 n 120 115 126 120 115 SD 77. total and HDL cholesterol.01). The mean fasting glucose level was 201 and 210 mg/dl in participants with NPR and PDR.0 20. risk factors were similar to our findings among the Sioux Indians. the no retinopathy and NPR categories were combined into one group. PDR). respectively.1 100 the categorical variables of renal dialysis (yes or no) and level of retinopathy (no retinopathy.8 2.3 2. 560 for NPR. and renal disease. respectively This was significantly higher than 174 mg/dl in participants with no retinopathy. and PDR. VOLUME 20.001) (Table 2).135.5 12. However. This may be due to the small sample size and/or characteristics of this population.9% in participants with no retinopathy and NPR. Photos deemed ungradable as either having no retinal detail. We identified similar risk factors.3 years. intravascular microvascular abnormalities without microaneurysms. prevalence studies in the Hispanic population of San Luis Valley using this classification scheme are comparable (12).259. and 53. dialysis. dBP. however. as compared with 14.9 7. P = 0. poor field definition. (9-12) and U. Rates reported in studies of other U.1 6.4% and found duration of diabetes. renal disease. diastolic blood pressure (dBP).3 17.2 and 5. West et al. duration of diabetes. Fishers exact probability test was used to examine the relationship between Table 2—Factors associated with retinopathy (P < 0. 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. plasma triglyceride level. using the modified Airlie House Classification Scheme (8).5 2. sex. with 40. 1%. Fasting blood glucose. NPR. Five factors were identified as being associated with severity of retinopathy (P < 0.1 1. C O N C L U S I O N S — The prevalence of diabetic retinopathy among this group of diabetic Sioux Indians was 45.8 116 7.9 758 DIABETES CARE. NPR.807 in participants with PDR. HbA lc .7 40.5 n 14 14 16 14 16 SD 79. Age was found not to be a risk factor. All readable photos were graded as follows: no retinopathy.7% and 8. blood cholesterol.2 5. Our appropriate treatment.807 14.5 31.4 NPR Mean 209. fasting glucose. Approximately 45.3% of the peoples eyes whose photos were evaluated had diabetic retinopathy.6 53. therefore. and 124 mmHg for no retinopathy The UACR was 1.3 142. We found age. sBP.3% in PDR vs. Logistic regression was not used because missing information for some of the important variables resulted in equations with only about 100 cases.Diabetic retinopathy among Sioux Indians Table 1—Presence of diabetic retinopathy Percentage No retinopathy NPR PDR Total 226 166 21 413 54. it could be underestimated. triglyceride levels were not evaluated in our study Another study among Oklahoma Indians (Cheyenne-Arapaho) reported prevalence rates of diabetic retinopathy to be 49.9 130. stroke. exercise. systolic blood pressure (sBP). or microaneurysms only).1 2. Our assessment of stroke was based on patient history and/or clinic charts.05 were considered to be statistically significant.9 8. history of stroke.3%.
MD. Elisa Lee. Bennett J. Savage PJ. Fabsitz RR. In Diabetes in America. 1987 DIABETES CARE. Yeh JL.16. 11. Creeks (Oklahoma) (13) Cheyenne-Arapaho (Oklahoma) (14) Pima (Arizona) Hispanic (San Luis Valley. including the Black Hills Regional Eye Institute. Mary Buurma. van Hcuvcn WAJ. age at diagnosis of diabetes. Owing to limited resources and equipment. and renal disease as being significant risk factors. Texas (9) South-central Wisconsin (NIDDM only) (11) Number studied Rate (%) 417 142 973 1. Leonardson is currently with Mountain Plains Research. Cheyenne-Arapaho. Welty TK. D. Kaufman S. no. Gohdes D. duration of diabetes. Diabetes Care 18:599-610.J. Robbins DC. thereby preserving vision and preventing blindness. the prevalence of diabetic retinopathy could be reduced. U.C. Invest Ophthalmol Vis Sci 21:210-226. Welty TK: Diabetes mellitus and impaired glucose tolerance in three Ameri. whose presence is missed by all who worked with him. Klein BEK. Welty TK: Coronary heart disease prevalence and its relation to risk factors in American Indians: The Strong Heart Study. Am] Epidemiol 142:254-268. D.640 279 257 1. 9. 1976 The Diabetes Control and Complications Trial Research Group: Color photography vs. Yeh JL. Department of Ophthalmology for grading the fundus photos. and age at examination in a population with a high prevalence of diabetes mellitus. Klein R: Diabetic retinopathy in Mexican Americans and non-Hispanic whites.. MPH. 1986 2. Klein R. DeMets DL: The Wisconsin Epidemiologie Study of Diabetic Retinopathy. 1984 Klein R. Valway S. The high prevalence of retinopathy also stresses the need for annual eye examinations in this population. Cowan LD. Dicibetes 37:878-884. 1995 Diabetic Retinopathy Study Research Group. Cowan LD. 1989 West KW. Patterson JK. References 1. Parsley TL: The prevalence and risk of diabetic retinopathy among Indians of Southwest Oklahoma. MD. Diabetes Care 9:609-613. Howard WJ. Gohdes DM: Diabetes in American Indians: a growing problem. South Dakota. Miller M: Retinopathy in Pima Indians: relationships to glucose level. We would like to thank the participants of the study. Berinstein is currently at The New York Eye and Ear Infirmary.370 45 24 49 18 42 45 39 7. Diabetes 25:554-560. while serving Indian patients. OD. 95-1468) 5.15. 1995 (NIH publ. II. Hazuda HP. and J. Arch Ophthalmol 102:527-532. and Nebraska. Oopik AJ. MAY 1997 759 .S. By implementing aggressive glycemic and blood pressure control. Dici/?r(t\s 29:501-508. Freeman W. Diabetes 38:1231-1237. 111. Moo-Young GA. ~ 2 0 % of patients with no retinopathy had evidence of retinopathy on fluorescein angiogram (16). Cucchiara AJ. Am J Epidemiol 132:1141-1155. Stober JA: A detailed study of risk factors for retinopathy and nephropathy in diabetes. 1993 3. Herlihy is currently in private practice. NY. In conclusion. Montana. Klein BEK. Valway SE: Diabetes 14. Hildebrandt W Marshall JA. The Diabetes Control and Complications Trial Research Group showed that with use of color photographs alone. protocol of two photographs for each eye and of the use of color photographs alone may underestimate the prevalence of retinopathy in this population. Walsh. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Robbins DC. Bozeman. 1989 Dorf A. duration of diabetes. VOLUME 20.M. Cowan LD. Go O. Acknowledgments — The opinions expressed in this paper are ours and do not necessarily reflect the views of the Indian Health Service. sBP. 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. 8. Stem MP. Klein B: Vision disorders in dia. 1984 Hamman RF. Oopik AJ.. the estimated prevalence rate of diabetic retinopathy among the Sioux Indians is 45. The modified Airlie House classification defines seven standard stereo photographic fields in classifying retinopathy (8). North Dakota.13. Howard BV: The Strong Heart Study: a study of cardiovascular disease in American Indians: design and methods. G. Seminoles. Gohdes D: Prevalence of diagnosed diabetes among American Indi. Helgerson SD.R. Moss SE: The Wisconsin Epidemiologie Study of diabetic retinopathy. Report VII: a modification of the Airlie House classification of diabetic retinopathy. PhD. 1980 Newell SW Tolbert B. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. The University of Wisconsin School of Medicine 12. PhD. NUMBER 5. Kiowas. MD. Ballantine EJ. These results are reflective of the health needs of the Sioux Indian population. with fasting blood glucose. Davis MD. HbA lc . Fabsitz RR. Lee ET. Colorado) (12) San Antonio. and Joseph Hartford. 10.3%. Fabsitz R. This paper is in honor of Ruggles Stahn. Arch Ophthalmol 102:520-526. Moss SE. 1981 Haffner SM. Richard Fabsitz. 14 photographs for each patient were not feasible. 1990 Howard BY Lee ET. Le NA. in a tragic plane crash in Minot. for their invaluable comments. Rapid City. l):244-247. and Joseph B. New York. Barbara Howard. 1994. Oopik AJ. Washington. Fong D. Stahn RM. Lee ET. 1995 6. 1993 4. Baxter J: Prevalence and risk factors of diabetic retinopathy in non-Hispanic Whites and Hispanics with NIDDM: San Luis Valley Diabetes Study. South Dakota. Printing Office. Govt. Pugh JA. Erdreich LJ. J Okla State Med Assoc 82:414-423. Bennett PH. ans and Alaska Natives. Mayer EJ.Berinstein and Associates Table 3—Prevalence rates of diabetic retinopathy in NIDDM diabetic populations Population Sioux (South Dakota) Comanches. betes. 2nd ed. Savage PJ. Howard BV Savage PJ. 1988 Klein R. can Indian populations aged 45-74 years: The Strong Heart Study. PAC. l):271-276. Welty T. He died February 18. Richard Devereux. and its complications among selected tribes in North Dakota. 1987: estimates from a national outpatient data base. fluorescein angiography in the detection of diabetic retinopathy in the Diabetes Control and Complications Trial. Diabetes Care 6 (Suppl. Diabetes Care 16 (Suppl. Such intervention will allow early diagnosis and treatment. Arch Ophthalmol 105:1344-1351.
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