Skip to main content
Experimental Diabetes Research logoLink to Experimental Diabetes Research
. 2008 Jan 16;2007:76271. doi: 10.1155/2007/76271

Diabetic Retinopathy in Native and Nonnative Canadians

Stuart A Ross 1,*, Anne McKenna 1, Sheila Mozejko 2, Gordon H Fick 3
PMCID: PMC2248248  PMID: 18317512

Abstract

High prevalence rates of type 2 diabetes are being observed in native Canadian communities. It is believed that native populations have a higher prevalence rate of vascular complications than nonnatives. The Southern Alberta Study of Diabetic Retinopathy (DR) examined the prevalence and incidence of DR and associated metabolic abnormalities in native and nonnative subjects. Prevalence rates of DR in type 2 diabetic native and nonnative subjects were identical, with a prevalence rate of 40%. Native subjects with retinopathy, however, tended to have more advanced changes of retinopathy compared to the nonnative subjects. Key factors such as A1c, blood pressure, duration of diabetes, and lipid values were not significantly different between the two cohorts. These data indicate that ethnicity does play a role in the development and severity of DR but potential risk factors that may affect the development of retinopathy are not significantly different between native and nonnative groups.

1. INTRODUCTION

Diabetic retinopathy remains an important cause of visual loss in persons with diabetes. As the prevalence rates of diabetes increase in both the native and nonnative populations, there is increasing concern of the potential increased numbers of patients at risk for diabetic retinopathy. Some potential risk factors for retinopathy include: A1c, BP (systolic and diastolic), and duration of diabetes [15]. Lipid abnormalities may also play part in the development of retinal changes [6].

It is often assumed that native populations have different prevalence rates of specific vascular complications and of the risk factors that may lead to the development of vascular complications. This paper reviews the prevalence rates of diabetic retinopathy in native and nonnative communities and directly compares the prevalence rates of potential risk factors for the development of diabetic retinopathy in these communities.

2. METHODOLOGY

The Southern Alberta Study of Diabetic Retinopathy (SASDR) was designed to provide assessment of the prevalence and incidence of diabetic retinopathy and other diabetes vascular complications and to assess potential risk factors for the development of retinopathy in a population of subjects with diabetes. Native and nonnative communities were assessed as part of the study. The study was carried out in southern Alberta and included both urban and rural areas and native reserves. At a minimum of three years following the completion of the initial prevalence study, all subjects were invited to take part in the incidence study, which repeated all parameters of the prevalence programme. This paper will review only the prevalence data.

All subjects were identified as either urban (Calgary) or rural, by the postal codes associated to their place of primary residence. Within the borders of the study area, there are six native reserves belonging to Treaty Seven, including the two largest native reserves in Canada, the Blood and Blackfoot reserves. The project was approved by (The Conjoint Health Research Ethics Board, University of Calgary, Canada) and by the medical committees of each of the native reserves. All southern Alberta reserves were represented in the study and are shown in Table 1.

Table 1.

Southern Alberta native reserves-treaty seven.

Reserve Tribe
Blood Blackfoot
Piikani Blackfoot
Blackfoot Blackfoot
Morley Stoney
Eden Valley Stoney
TsuuTina Sarcee

2.1. Recruitment

Insulin-using subjects —

Registration centers were established across the study area of southern Alberta. These included all pharmacies, physicians’ offices, nursing homes, auxiliary hospitals, native reserves and prisons. Each recruitment site had information and registration packages and staff was individually trained to administer the package to all subjects who used insulin.

Noninsulin-using subjects —

The same techniques of registration could not be used for the noninsulin-using subjects as many may not use drugs or have the need to go into a pharmacy. Recruitment of the noninsulin-using subjects began after the identification of the insulin-using subjects. The family physician of each insulin-using subject registered in the study was provided with the number of insulin users registered from their practice and requested to invite the next and subsequent patients with noninsulin-using diabetes within the practice, to register for the study. Each recruitment site that had recruited insulin-using subjects was similarly asked to recruit an equal number of noninsulin-using subjects.

Nonparticipants —

At each of the recruitment sites, if the diabetic subject refused to complete the registration card, the gender, approximate age of the subject, and the specific reason for the refusal was documented.

2.2. Assessment

Assessment of the individual subjects was undertaken in multiple sites. For those who lived in Calgary, participants attended the central SASDR office at the University of Calgary. For those who could not attend in Calgary, remote sites were set up across southern Alberta. At regular intervals, a mobile van was utilized to carry the staff and retinal and blood sampling equipment to the sites. Subjects were asked to complete an extensive 20-page questionnaire which included a review of ethnic origin, family, and personal medical history with a special emphasis on the history of diabetes, data of diagnosis, drug treatments, and existing vascular complications. A basic examination was performed, including height and weight for calculation of BMI; systolic blood pressure (BP-S) and diastolic blood pressure (BP-D). Each subject was also asked to provide a timed-overnight urine sample and a venous blood sample. Type 2 insulin-using subjects were identified by a serum C-peptide > 0.05 nmol/L.

Ophthalmology assessment —

Each subject had a complete ophthalmology assessment including visual acuity, examination for cataracts, seven-field stereofundus retinal photography, and a slit lamp examination. The photographic slides were coded and forwarded to (Wisconsin Eye Reading Center, Wis, USA) for the classification of the degree of diabetic retinopathy according to the Airlie House classification as adapted by R. Klein et al. [7] Table 2.

Table 2.

Retinal grade classification.

Grade Description
10–14 no retinopathy
15–21 microaneurysms or soft exudates or retinal hemorrhages
31 micro aneurysms with any of: venous loops; soft exudates; intraretinal microvascular abnormalities (IRMA); venous beading; retinal hemorrhages
41 microaneurysms with any of the following: hemorrhages and 4-5 fields; IRMA 1–3 fields
51 microaneurysms with one or more of the following: hemorrhages and microaneurysms in 4-5 fields; IRMA in 4 or more fields; venous beading in 2 or more fields
60 fibrous proliferations
61 scars of photocoagulation but no evidence of 60 or 65
65 proliferative retinopathy

Laboratory investigations —

A venous blood sample was obtained for the measurement of a nonfasting lipid profile; A1c; serum creatinine; glucose; and serum C-peptide (for assessment of insulin-dependency). The urine sample was assessed for the presence of microalbuminuria and for the presence of ketones. The microalbumin-excretion rate was measured from a timed-overnight urine sample.

Statistical analysis —

To describe the association of ethnicity with retinopathy and potential risk factors, chi-squared tests were used to compare rates and t-tests were used to compare means. All testing was done at the 0.05 level of significance.

3. RESULTS

Retinopathy versus no retinopathy for native versus nonnative subjects —

There were a total of 2247 patients with Type 2 diabetes, 232 were native and 2015 were nonnative. Table 3 describes the breakdown of patients by ethnicity and retinopathy as follows.

Table 3.

Prevalence of diabetic retinopathy.

Native Nonnative Total
No retinopathy 137 (60%) 1208 (60%) 1345 (60%)
retinopathy 91 (40%) 805 (40%) 895 (40%)

Total 228 (100%) 2013 (100%) 2241(100%)

The results of a Chi-Squared test for the equality of the retinopathy rates, (χ 2 = 0.0005 with 1 degree of freedom, P = .98) indicate that ethnicity appears to play no role on the incidence of retinopathy for patients with Type 2 diabetes.

The question of whether ethnicity is related to the degree of retinopathy is described in Table 4 as follows.

Table 4.

Degree of retinopathy.

Native Nonnative Total
Background 45 (49%) 551 (68%) 596 (67%)
Preproliferative 33 (36%) 174 (22%) 207 (23%)
Proliferative 13 (14%) 80 (10%) 93 (10%)

Total 91 (100%) 805 (100%) 896 (100%)

The Chi-Square test for independence (χ 2 = 13.52 with 2 degrees of freedom, P = .0002) indicates that there is a strong relationship between ethnicity and the degree of retinopathy for patients with Type 2 diabetes. If the patient is native there is a good chance that his/her retinopathy will be more severe than if the patient was nonnative.

Risk factors for retinopathy —

Table 5 provides a breakdown of these factors relative to native/nonnative classifications as follows.

The native subjects had poorer glucose control with significantly higher levels of A1c compared to the nonnative subjects. There were small but significant differences between native and nonnative subjects in measurements of diastolic blood pressure. Native subjects showed significantly better lipid profiles compared to the nonnative subjects. There were no significant differences in systolic blood pressure measurements or duration of diabetes between the two groups.

Table 5.

Risk factors for diabetic retinopathy.

Factor Observations Average Standard deviation P
Native Nonnative Native Nonnative Native Nonnative
A1c 224 2010 7.52 7.15 2.0 1.78 .008
BP-S mm/Hg 228 2010 129 130 21.59 19.07 .3611
BP-D mm/Hg 228 2010 78 75 10.27 10.11 .0025
Total-Cholesterol mmol/L 225 2011 5.4311 5.5454 1.12 1.32 .0274
HDL-C mmol/L 225 2007 1.1748 1.056 0.37 0.32 <.0005
Duration years 221 1981 8.26 9.08 7.13 8.42 .164

Tables 69 investigate the risk factors with degree of retinopathy. Each table is broken down by the risk factor and native/nonnative categories. Ret 1 is no retinopathy; Ret 2 is background retinopathy; Ret 3 is preproliferative retinopathy; and Ret 4 is proliferative retinopathy.

Table 6.

No retinopathy and associated risk factors.

Ret1 Observations Average Standard deviation P
Native Nonnative Native Nonnative Native Nonnative
A1c 134 1205 7.20 6.85 1.89 1.67 .0455
BP-S mm/Hg 137 1205 125 127 18.3 17.8 .1262
BP-D mm/Hg 137 1205 77 75 9.2 10 .0544
Total-Cholesterol mmol/L 135 1206 5.323 5.533 1.02 1.32 .0733
HDL-C mmol/L 135 1202 1.182 1.055 0.385 0.312 .003
Duration years 133 1190 5.962 7.086 5.95 7.65 .1015

Table 9.

Proliferative retinopathy and associated risk factors.

Ret4 Observations Average Standard deviation P
Native Nonnative Native Nonnative Native Nonnative
A1c 12 80 8.76 7.88 2.55 1.55 .2596
BP-S mm/Hg 13 80 147 136 32.4 20.7 .2577
BP-D mm/Hg 13 80 80 76 13.8 12.7 .2593
Total-Cholesterol mmol/L 12 80 5.7108 5.546 1.17 1.31 .6828
HDL-C mmol/L 12 80 1.113 1.01 0.338 0.249 .208
Duration years 13 80 16.769 15.4 9.2 9.25 .6217

Native subjects had significantly higher A1c values with minor differences in the other parameters Table 6.

Native subjects had significantly higher BP-D; HDL-C values; and shorter duration of diabetes Table 7.

Table 7.

Background retinopathy and associated risk factors.

Ret2 Observations Average Standard deviation P
Native Nonnative Native Nonnative Native Nonnative
A1c 45 551 7.74 7.37 1.77 1.67 .1596
BP-S mm/Hg 45 551 131 133 20.5 19.9 .662
BP-D mm/Hg 45 551 80 76 11.3 9.9 .01
Total-Cholesterol mmol/L 45 551 5.282 5.513 1.01 1.26 .2291
HDL-C mmol/L 45 551 1.178 1.076 0.391 0.335 .0524
Duration years 40 535 8.6 11.215 5.56 8.51 .0564

There were no clinically significant differences between the native and nonnative groups apart from significantly higher HDL-C values in native subjects Table 8.

Table 8.

Preproliferative retinopathy and associated risk factors.

Ret3 Observations Average Standard deviation P
Native Nonnative Native Nonnative Native Nonnative
A1c 33 174 8.03 8.17 2.0 1.89 .7006
BP-S mm/Hg 33 174 77 77 11.4 10.1 .965
BP-D mm/Hg 33 174 133 137 26.3 20.6 .4216
Total-Cholesterol mmol/L 33 174 5.376 5.731 1.6 1.53 .2254
HDL-C mmol/L 33 174 1.166 1.022 0.302 0.297 .0119
Duration years 33 174 13.939 13.362 6.99 8.24 .7064

While the mean values in the native group for A1c, blood pressure readings, lipids, and duration are higher than the nonnative groups, there were no significant differences between the two subject groups Table 9.

The most frequent differences in risk factors between native and nonnatives are at the “no retinopathy” stage and the “background” stage. Once a patient has preproliferative or proliferative disease, there is very little or no difference in risk factors regardless of ethnicity.

4. DISCUSSION

The prevalence of diabetes is increasing worldwide. Associated with this increase is an increased risk of development of micro- and macrovascular complications including diabetic retinopathy. Aboriginal or native communities may be at increased risk of developing prediabetes or type 2 diabetes. There may well be an increased risk of microvascular complications amongst these communities [813].

Native communities in north America have previously been identified as having an increased risk of type 2 diabetes [14]. While the risk of developing type 2 diabetes may vary between various native-Canadian nations, many are exhibiting an increased prevalence rate of type 2 diabetes [13, 1521]. Detailed studies of (Ojibwa-Cree native populations in Sandy Lake, Ontario, Canada) have revealed increased prevalence rates of impaired glucose tolerance as well as type 2 diabetes [8, 10, 22]. Similar abnormalities have been noted in (James Bay Cree in northern Québec, Canada) [19].

Native Canadians have also been identified as having increased morbidity and mortality associated with diabetes with a greater impact on quality of life and a strong association between diabetes, hypertension, heart disease, and sight impairment [9]. Renal disease is also more prominent with an increased prevalence rate of diabetic end-stage renal disease evident in native Canadians [2326].

There are only a limited number of studies related to diabetic retinopathy in native populations. In Canada particularly, many native populations are in remote areas and extensive studies have proven to be difficult. Increased vascular complications, including diabetic retinopathy, have been noted in the James Bay Cree and other native populations [24, 25, 27, 28]. Haffner et al. noticed an increase prevalence rate of diabetic retinopathy in Mexican-American diabetic subjects compared to Caucasian diabetic subjects reviewed in (Wisconsin Epidemiologic Study of Diabetes, Wis, USA) suggesting an ethnicity effect on the risk of developing diabetic retinopathy [29]. Studies of the Pima Indians have shown a similar increase in prevalence rates [30]. An urban study, however, carried out in the native population in Vancouver, showed that visual disability was nine times greater than in the general Canadian population but diabetic retinopathy was not a major cause of that visual loss [31].

Various risk factors have been identified as leading to an increased incidence of diabetic retinopathy. These include glycemic control [4, 5, 3235], elevated blood pressure [3, 33, 3638], abnormal lipids [39, 40], and duration of diabetes [41]. It is thought that native Canadians may exhibit higher prevalence rates of these risk factors, compared to nonnative individuals. Detailed studies of native-north Americans have revealed high prevalence rates of these risk factors. A review of Sandy Lake community demonstrated high prevalence rates of vascular complications and associated risk factors [8, 11]. Studies of other native Canadian communities have revealed similar results [18, 42, 43].

The prevalence data from the Southern Alberta Study of Diabetic Retinopathy (SASDR) provides a unique opportunity to review prevalence rates of diabetic retinopathy, severity and the potential associated risk factors for the development of retinopathy directly between insulin and noninsulin using type 2 diabetic native and nonnative subjects.

As can be seen from the data presented, there were no differences in prevalence rates of retinopathy between the native and nonnative groups. Native subjects with retinopathy, however, tended to have more advanced changes of retinopathy compared to the nonnative subjects.

When assessing the role of potential risk factors for the development or progression of diabetic retinopathy, again, there were only few and minor differences between native and nonnative subjects. Both native and nonnative subjects with more severe presentation of diabetic retinopathy tended to have higher levels of A1c compared to those with less severe forms of retinopathy. Significantly higher levels of A1c were observed only in native subjects who did not exhibit retinopathy. A1c was not statistically significant for patients with some form of retinopathy. Native subjects tended to have lower total-cholesterol and higher HDL-C values compared to nonnative groups although these differences were small. Duration of diabetes, which is recognized as a major risk factor for the development and severity of diabetic retinopathy, was not significantly different between native and nonnative subjects.

Of interest are the differences in prevalence and severity of diabetic retinopathy in the southern Alberta native subjects compared to those from the detailed Sandy Lake study [11]. The prevalence rates of retinopathy were far higher in the southern Alberta cohort and similar to those identified in the Wisconsin Eye Studies [44].

These data indicate that ethnicity does play a significant role in the development and severity of diabetic retinopathy but potential risk factors that may accelerate the development of retinopathy are not significantly different between native and nonnative groups.

ACKNOWLEDGMENTS

The authors would like to acknowledge Dr. Ron Klein for his continuous support and advice throughout the SASDR project. They would like to acknowledge the Lions Club District 37E, Alberta; NHRDP, and the Kahanoff Foundation for generous grant support.

References

  • 1.Klein BE, Klein R, Moss SE, Palta M. A cohort study of the relationship of diabetic retinopathy to blood pressure. Archives of Ophthalmology. 1995;113(5):601–606. doi: 10.1001/archopht.1995.01100050069033. [DOI] [PubMed] [Google Scholar]
  • 2.Klein BE, Klein R, Moss SE, Palta M. Erratum: a cohort study of the relationship of diabetic retinopathy to blood pressure. Archives of Ophthalmology. 1995;114(1):109. doi: 10.1001/archopht.1995.01100050069033. [DOI] [PubMed] [Google Scholar]
  • 3.Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. Is blood pressure a predictor of the incidence or progression of diabetic retinopathy? Archives of Internal Medicine. 1989;149(11):2427–2432. [PubMed] [Google Scholar]
  • 4.Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. Glycosylated hemoglobin predicts the incidence and progression of diabetic retinopathy. Journal of the American Medical Association. 1988;260(19):2864–2871. [PubMed] [Google Scholar]
  • 5.Klein BE, Moss SE, Klein R. Longitudinal measure of glycemic control and diabetic retinopathy. Diabetes Care. 1987;10(3):273–277. doi: 10.2337/diacare.10.3.273. [DOI] [PubMed] [Google Scholar]
  • 6.Chew EY, Klein ML, Ferris FL, III, et al. Association of elevated serum lipid levels with retinal hard exudate in diabetic retinopathy: early treatment diabetic retinopathy study (ETDRS) report 22. Archives of Ophthalmology. 1996;114(9):1079–1084. doi: 10.1001/archopht.1996.01100140281004. [DOI] [PubMed] [Google Scholar]
  • 7.Klein R, Klein BE, Moss SE, Cruickshanks KJ. The Wisconsin epidemiologic study of diabetic retinopathy: XIV. Ten-year incidence and progression of diabetic retinopathy. Archives of Ophthalmology. 1994;112(9):1217–1228. doi: 10.1001/archopht.1994.01090210105023. [DOI] [PubMed] [Google Scholar]
  • 8.Harris SB, Zinman B, Hanley A, et al. The impact of diabetes on cardiovascular risk factors and outcomes in a native Canadian population. Diabetes Research and Clinical Practice. 2002;55(2):165–173. doi: 10.1016/s0168-8227(01)00316-3. [DOI] [PubMed] [Google Scholar]
  • 9.Bruce SG. The impact of diabetes mellitus among the Métis of western Canada. Ethnicity & Health. 2000;5(1):47–57. doi: 10.1080/13557850050007347. [DOI] [PubMed] [Google Scholar]
  • 10.Harris SB, Gittelsohn J, Hanley A, et al. The prevalence of NIDDM and associated risk factors in native Canadians. Diabetes Care. 1997;20(2):185–187. doi: 10.2337/diacare.20.2.185. [DOI] [PubMed] [Google Scholar]
  • 11.Hanley AJG, Harris SB, Mamakeesick M, et al. Complications of type 2 diabetes among aboriginal Canadians: prevalence and associated risk factors. Diabetes Care. 2005;28(8):2054–2057. doi: 10.2337/diacare.28.8.2054. [DOI] [PubMed] [Google Scholar]
  • 12.Ekoe J-M, Thouez J-P, Petitclerc C, Foggin PM, Ghadirian P. Epidemiology of obesity in relationship to some chronic medical conditions among Inuit and Cree Indian populations in New Quebec, Canada. Diabetes Research and Clinical Practice. 1990;10(1):S17–S27. doi: 10.1016/0168-8227(90)90135-g. [DOI] [PubMed] [Google Scholar]
  • 13.Macaulay AC, Montour LT, Adelson N. Prevalence of diabetic and atherosclerotic complications among Mohawk Indians of Kahnawake, PQ. Canadian Medical Association Journal. 1988;139(3):221–224. [PMC free article] [PubMed] [Google Scholar]
  • 14.Bennett PH, Rushforth NB, Miller M, LeCompte PM. Epidemiologic studies of diabetes in the Pima Indians. Recent Progress in Hormone Research. 1976;32:333–376. doi: 10.1016/b978-0-12-571132-6.50021-x. [DOI] [PubMed] [Google Scholar]
  • 15.Evers S, McCracken E, Antone I, Deagle G. The prevalence of diabetes in Indians and Caucasians living in Southwestern Ontario. Canadian Journal of Public Health. 1987;78(4):240–243. [PubMed] [Google Scholar]
  • 16.Montour LT, Macaulay AC. High prevalence rates of diabetes mellitus and hypertension on a North American Indian reservation. Canadian Medical Association Journal. 1985;132(10):1110–1112. [PMC free article] [PubMed] [Google Scholar]
  • 17.Harris SB, Gittelsohn J, Hanley A, et al. The prevalence of NIDDM and associated risk factors in native Canadians. Diabetes Care. 1997;20(2):185–187. doi: 10.2337/diacare.20.2.185. [DOI] [PubMed] [Google Scholar]
  • 18.Young TK, Harris SB. Risk of clinical diabetes in a northern Native Canadian cohort. Arctic Medical Research. 1994;53(2):64–70. [PubMed] [Google Scholar]
  • 19.Brassard P, Robinson E, Lavallee C. Prevalence of diabetes mellitus among the James Bay Cree of northern Quebec. Canadian Medical Association Journal. 1993;149(3):303–307. [PMC free article] [PubMed] [Google Scholar]
  • 20.Dean HJ, Mundy RL, Moffatt M. Noninsulin-dependent diabetes mellitus in Indian children in Manitoba. Canadian Medical Association Journal. 1992;147(1):52–57. [PMC free article] [PubMed] [Google Scholar]
  • 21.Szathmary EJE, Holt N. Hyperglycemia in Dogrib Indians of the Northwest territories, Canada: association with age and a centripetal distribution of body fat. Human Biology. 1983;55(2):493–515. [PubMed] [Google Scholar]
  • 22.Young TK. Diabetes mellitus among native Americans in Canada and the United States: an epidemiological review. American Journal of Human Biology. 1993;5(4):399–413. doi: 10.1002/ajhb.1310050405. [DOI] [PubMed] [Google Scholar]
  • 23.Young TK, Kaufert JM, McKenzie JK, Hawkins A, O'Neil J. Excessive burden of end-state renal disease among Canadian Indians: a national survey. American Journal of Public Health. 1989;79(6):756–758. doi: 10.2105/ajph.79.6.756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Dyck PJ, Kratz KM, Karnes JL, et al. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology. 1993;43(4):817–824. doi: 10.1212/wnl.43.4.817. [DOI] [PubMed] [Google Scholar]
  • 25.Dyck PJ, Kratz KM, Karnes JL, et al. Erratum: the prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology. 1993;43(11):2345. doi: 10.1212/wnl.43.4.817. [DOI] [PubMed] [Google Scholar]
  • 26.Dyck RF, Tan L. Rates and outcomes of diabetic end-stage renal disease among registered native people in Saskatchewan. Canadian Medical Association Journal. 1994;150(2):203–208. [PMC free article] [PubMed] [Google Scholar]
  • 27.Brassard P, Robinson E, Dumont C. Descriptive epidemiology of noninsulin-dependent diabetes mellitus in the James Bay Cree population of Quebec, Canada. Arctic Medical Research. 1993;52(2):47–54. [PubMed] [Google Scholar]
  • 28.Martin JD, Yidegiligne HM. Diabetes mellitus in the first nations population of British Columbia, Canada. International Journal of Circumpolar Health. 1998;57(1):335–339. [PubMed] [Google Scholar]
  • 29.Haffner SM, Mitchell BD, Moss SE, et al. Is there an ethnic difference in the effect of risk factors for diabetic retinopathy? Annals of Epidemiology. 1993;3(1):2–8. doi: 10.1016/1047-2797(93)90003-m. [DOI] [PubMed] [Google Scholar]
  • 30.Nagi DK, Pettitt DJ, Bennett PH, Klein R, Knowler WC. Diabetic retinopathy assessed by fundus photography in Pima Indians with impaired glucose tolerance and NIDDM. Diabetic Medicine. 1997;14(6):449–456. doi: 10.1002/(SICI)1096-9136(199706)14:6<449::AID-DIA367>3.0.CO;2-D. [DOI] [PubMed] [Google Scholar]
  • 31.Maberley DAL, Hollands H, Chang A, Adilman S, Chakraborti B, Kliever G. The prevalence of low vision and blindness in a Canadian inner city. Eye. 2007;21(4):528–533. doi: 10.1038/sj.eye.6702257. [DOI] [PubMed] [Google Scholar]
  • 32.Dorf A, Ballintine EJ, Bennett PH, Miller M. Retinopathy in Pima Indians. Relationships to glucose level, duration of diabetes, age at diagnosis of diabetes, and age at examination in a population with a high prevalence of diabetes mellitus. Diabetes. 1976;25(7):554–560. doi: 10.2337/diab.25.7.554. [DOI] [PubMed] [Google Scholar]
  • 33.Teuscher A, Schnell H, Wilson PWF. Incidence of diabetic retinopathy and relationship to baseline plasma glucose and blood pressure. Diabetes Care. 1988;11(3):246–251. doi: 10.2337/diacare.11.3.246. [DOI] [PubMed] [Google Scholar]
  • 34.Klein BE, Klein R. Diabetic retinopathy: possible etiological role of hyperglycemia. Pediatrician. 1990;17(3):177–182. [PubMed] [Google Scholar]
  • 35.The diabetes control, complications trial research group The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. New England Journal of Medicine. 1993;329(14):977–986. doi: 10.1056/NEJM199309303291401. [DOI] [PubMed] [Google Scholar]
  • 36.Gæde P, Vedel P, Larsen N, Jensen GVH, Parving H-H, Pedersen O. Multifactorial intervention and cardiovascular disease in patients with type 2 diabetes. New England Journal of Medicine. 2003;348(5):383–393. doi: 10.1056/NEJMoa021778. [DOI] [PubMed] [Google Scholar]
  • 37.Klein R, Klein BE, Moss SE, Wang Q. Blood pressure, hypertension and retinopathy in a population. Transactions of the American Ophthalmological Society. 1993;91:207–226. [PMC free article] [PubMed] [Google Scholar]
  • 38.Lewis JM, Jovanovic-Peterson L, Ahmadizadeh I, Bevier W, Peterson CM, Williams B. The Santa Barbara County diabetic retinopathy screening feasibility study: significance of diabetes duration and systolic blood pressure. Journal of Diabetes and Its Complications. 1994;8(1):51–54. doi: 10.1016/1056-8727(94)90011-6. [DOI] [PubMed] [Google Scholar]
  • 39.Klein BE, Moss SE, Klein R, Surawicz TS. Serum cholesterol in Wisconsin epidemiologic study of diabetic retinopathy. Diabetes Care. 1992;15(2):282–287. doi: 10.2337/diacare.15.2.282. [DOI] [PubMed] [Google Scholar]
  • 40.Klein BE, Moss SE, Klein R, Surawicz TS. The Wisconsin epidemiologic study of diabetic retinopathy XIII. Relationship of serum cholesterol to retinopathy and hard exudate. Ophthalmology. 1991;98(8):1261–1265. doi: 10.1016/s0161-6420(91)32145-6. [DOI] [PubMed] [Google Scholar]
  • 41.Klein R, Klein BE, Moss SE. Epidemiology of proliferative diabetic retinopathy. Diabetes Care. 1992;15(12):1875–1891. doi: 10.2337/diacare.15.12.1875. [DOI] [PubMed] [Google Scholar]
  • 42.Howard BV, Magee MF. Diabetes and cardiovascular disease. Current Atherosclerosis Reports. 2000;2(6):476–481. doi: 10.1007/s11883-000-0046-8. [DOI] [PubMed] [Google Scholar]
  • 43.Delisle HF, Rivard M, Ekoe JM. Prevalence estimates of diabetes and of other cardiovascular risk factors in the two largest Algonquin communities of Quebec. Diabetes Care. 1995;18(9):1255–1259. doi: 10.2337/diacare.18.9.1255. [DOI] [PubMed] [Google Scholar]
  • 44.Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin epidemiologic study of diabetic retinopathy. III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Archives of Ophthalmology. 1984;102(4):527–532. doi: 10.1001/archopht.1984.01040030405011. [DOI] [PubMed] [Google Scholar]

Articles from Experimental Diabetes Research are provided here courtesy of Wiley

RESOURCES