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Risk factors for diabetic retinopathy in Latinos: Los Angeles Latino eye study
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Risk factors for diabetic retinopathy in Latinos: Los Angeles Latino eye study
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Content
RISK FACTORS FOR DIABETIC RETINOPATHY IN LATINOS: LOS
ANGELES LATINO EYE STUDY
Copyright 2004
by
Ginger Lee Macias
A thesis Presented to the
FACULTY OF THE GRADUATE SCHOOL
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
MASTER OF SCIENCE
(APPLIED BIOSTATISTICS/EPIDEMIOLOGY)
August 2004
Ginger Lee Macias
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UMI Number: 1422397
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ii
DEDICATION
I would like to dedicate this manuscript to my parents, Rafael and Jesselle Macias,
who have supported me, with love and encouragement, throughout this endeavor.
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iii
ACKNOWLEDGEMENTS
The writing of this thesis would not have been possible if not for the support and
encouragement of Dr. Stanley P. Azen. This year he was named “Professor of Year”
by the students for not only his teaching ability, but for his commitment to helping
students reach their potential. Thank you, Dr. Azen, for helping me realize my goals.
I would also like to thank Dr. Rohit Varma, Dr. Roberta McKean-Cowdin, Dr.
Fernando Pena, and the members of the Los Angeles Latino Eye Study Group.
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iv
TABLE OF CONTENTS
1. Dedication__________________________________________________ ii
2. Acknowledgments____________________________________________iii
3. List of Tables and Figures______________________________________ v
4. Abstract____________________________________________________vi
5. Introduction_________________________________________________ 1
6. Methods____________________________________________________ 2
a. Design________________________________________________2
b. Determination of Diabetes and Diabetic Retinopathy____________3
c. Risk Factors___________________________________________ 4
d. Statistical Analysis______________________________________ 5
7. Results_____________________________________________________ 6
a. Stratified Analyses Evaluating Sociodemographic Characteristics on
Increases in the Risk of Diabetic Retinopathy_________________ 13
b. Stratified Analyses Evaluating the Impact of Modifiable Variables on
the Risk of Diabetic Retinopathy___________________________ 14
8. Discussion__________________________________________________ 15
a. Comparisons with Other Studies___________________________16
b. Study Limitations______________________________________ 17
c. Conclusions___________________________________________17
9. Bibliography________________________________________________ 19
10. Appendices_________________________________________________22
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LIST OF TABLES AND FIGURES
Tables
1. Table 1. Univariate Associations with Any Diabetic Retinopathy.
2. Table 2. Stepwise Multivariable Model of Diabetic Retinopathy.
3. Table 3. Stepwise Multivariable of Proliferate Diabetic Retinopathy
Figures
1. Figure 1. Distribution of Diabetic Retinopathy in Type II Diabetics
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vi
ABSTRACT
A population-based cross-sectional study was conducted to identify risk factors
associated with diabetic retinopathy in Type II diabetic Latinos. An in-home
interview was administered to 6,357 Latinos aged 40 years and older in Los Angeles,
California. All participants diagnosed with diabetes underwent a complete
ophthalmologic examination.
46% of those with diabetes had diabetic retinopathy. Compared to females, males
had increased risk of DR (OR=1.37; 95%CI: 1.03-1.82). Factors increasing the risk
of DR were: having diabetes>15 years (OR=11.92; 95%CI: 7.19-19.74); hemoglobin
Ale levels>6.5% (OR=1.62; 95%CI: 1.07-2.46); blood glucose levels>200mg%
(OR=1.86; 95%CI: 1.28-2.72); diastolic blood pressure>90mmHg (OR=1.77; 95%
Cl: 1.13-2.77); insulin treatment (OR=1.58; 95%CI: 1.06-2.34). Modifiable factors
associated with increased risk of DR were: current smoking and obesity (p<0.10).
The increased risk of diabetic retinopathy in adult Latinos is due to risk factors
that have been associated among other populations, and risk was increased by several
modifiable factors. Further longitudinal studies investigating other mechanisms
should be conducted.
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1
INTRODUCTION
Diabetes mellitus (DM) has become one of the main public health challenges
for this century, especially because non-controlled DM results in cardiovascular and
systemic diseases.1 -4 In addition, extended duration of DM and high glycemic levels
5 7
diabetes may results in severe visual loss and blindness.'
Compared to African-Americans and Non-Hispanic Whites, it has been
o
shown that Latinos have a higher prevalence of DM and its complications.
Furthermore, Latinos with a Native-American ancestry have a higher prevalence of
DM than other Latinos9 and it is likely that Native-Americans have a higher
prevalence of ocular complications associated with DM. Retinopathy in individuals
with DM is the main complication that compromises the eye and is the leading cause
of new cases of blindness in the US. Several reports have found retinopathy to be
more prevalent in Latinos than in other ethnic groups.8 '1 0
The Los Angeles Latino Eye Study (LALES) is a population-based cross-
sectional study designed to determine the prevalence rates and risk factors associated
with blindness, visual impairment, and eye diseases, including diabetic retinopathy
(DR), in adult Latinos aged 40 years or older. In a recent report, we have reported
on the prevalence rates for DR in this population, and found that DR was the second
cause of visual impairment after cataracts, and the second cause of legal blindness
after age-related macular degeneration.1 1
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2
Various risk factors have been found associated with DR such as age, blood
pressure, inappropriate glycemic control, obesity and serum levels of cholesterol and
triglycerides.1 2 '1 4 Although these risk factors have been described in some studies
that included Latinos, it is not clear which factors play a role in the development of
DR in Latinos, as well as which risk factors are associated with the development of
advanced forms of DR, despite an apparent controlled glycemia.1 5
In this paper, we report on risk factors associated with various stages of DR
in the LALES cohort of Latinos diagnosed with having non-insulin dependent DM.
In addition, we compare these risk factors with those found in previous reports, and
contrast these factors with other risk factors, such as obesity, smoking, alcohol that
may be moderated in prevention programs.
METHODS
Design. The Los Angeles Latino Eye Study (LALES) consisted of self-identified
Latinos, aged 40 years or older, living in the City of La Puente, California. An in-
home questionnaire and a complete clinical and eye exam were administered to all
eligible participants. The University of Southern California’s Institutional Review
Board approved the study and all procedures were in accord with the standards of the
Declaration of Helsinki for research involving human subjects. An informed consent
was obtained from all study participants. Details of the study design, sampling plan,
and baseline data are reported elsewhere.1 1
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3
Determination of Diabetes and Diabetic Retinopathy. Participants were asked
about previous diagnoses of diabetes mellitus, and, if diagnosed, they were asked
about their treatment regimen (oral hypoglycemic medications, insulin, or diet
alone). Participants were newly diagnosed with definite diabetes during their clinic
visit if their hemoglobin Ale (HbAlc) was greater than or equal to 7.0%, or if their
random blood glucose level was greater than or equal to 200 mg%. All definite
cases of diabetes were considered to be Type II diabetes unless the participant was
diagnosed before the age of 30 and was being treated with insulin, which was
considered to be Type I diabetes. Random blood glucose and glycosylated
hemoglobin were measured using the Hemocue B-Glucose Analyzer (Hemocue Inc.,
Lake Forest, CA) and the DC A 2000+ System (Bayer Corporation, Tarrytown, NY),
respectively.
A series of detailed photographs of the fundus were obtained from those
individuals identified as having definite diabetes. Seven standard ETDRS fields of
the fundus for each eye were obtained using the Topcon TRC 50EX Retinal Camera
(Topcon Corporation of America, Paramus, NJ) using Kodak Ektachrome 100 film.
Complete details of these seven fields are explained elsewhere.1 6 The Ocular
Epidemiology Grading Center at the University of Wisconsin, Madison, WI, graded
the stereoscopic fundus photographs.
Diabetic retinopathy was defined as retinopathy in persons with definite
diabetes mellitus. Grading protocols for DR are modifications of the Early
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4
Treatment Diabetic Retinopathy Study (ETDRS) adaptation of the modified Arlie
House classification of DR.1 7 '1 9 Eyes were graded according to the following criteria:
1) no DR (levels 10 through 13); or 2) any DR (levels 14 through 85). Diabetic
retinopathy was then classified as 1) non-proliferative diabetic retinopathy (NPDR):
mild (level 14 through 20), moderate (levels 31 through 43), or severe (levels 47
through 53); or 2) proliferative diabetic retinopathy (PDR) (levels 60 through 85).
Risk Factors. Candidate risk factors for our analyses of diabetic retinopathy
included socio-demographic factors, health and vision insurance coverage, utilization
of vision and healthcare services, lifestyle risk factors, and clinical/ocular factors.
The in-home questionnaire provided the following socioeconomic and
demographic information: education, income, gender, age, country of birth, Native
American ancestry, and acculturation. An acculturation index was derived by asking
the participant several questions of primary language use, which included speaking,
reading, or writing in Spanish. General health service use was also obtained through
the in-home survey. For our analyses this included number of times in the past year
the participant visited a physician, and whether or not they had medical insurance.
During the in-home interview, the following clinical information was
obtained from the participant: previous diagnosis of diabetes, treatment of diabetes
and ocular disease history. Alcohol use and smoking patterns were also obtained at
this time. Questions pertaining to alcohol were categorized as ‘Never’, ‘Partial
drinker’, and ‘Regular drinker’ for our analysis. Participants were considered
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5
smokers if they smoked more than 100 cigarettes in their lifetime. In our study
smoking was categorized as ‘Never’, ‘Ex-smoker’, and ‘Current smoker’.
Clinical risk factors were obtained from the clinical exam, which included
weight, height, blood glucose level, HbAlc, albumin, creatinine, blood pressure, and
ocular assessments of prior cataract surgery, and measurements of spherical
equivalents.
Statistical Analysis. Chi-square analyses were conducted to assess the univariate
association of risk factors with any diabetic retinopathy (none vs. DR), and across
the diabetic retinopathy spectrum (none, NPDR and PDR). Those risk factors that
had a p-value <0.1 were considered as candidate risk factors for the multivariable
logistic regression model. Forward stepwise logistic regression procedures were
conducted, in which the risk factors were included in the model if the p-value was
<0.05. For validation purposes, logistic regression analyses were also run using the
backward elimination method.
Stratified Mantel-Haenszel analyses were conducted to evaluate differences
in risk factors identified in the multivariable analyses between subgroups defined by
sociodemographic variables (gender, income, education, and Native-American
ancestry) and modifiable variables (smoking, alcohol and obesity). Equivalency of
odds ratios across strata were tested using the Breslow-Day test of homogeneity of
the odds ratios at the 0.10 level. All analyses were performed using the Statistical
Analysis System (version 9.0, SAS Institute Inc, Cary, NC).
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RESULTS 6
Of the 6357 eligible participants who completed a clinical examination, 1263
participants had definite diabetes mellitus. 1187 subjects (94% of those with definite
diabetes) were identified as having Type II diabetes. Figure 1 shows the distribution
of diabetic retinopathy among confirmed Type II diabetics in our study population.
Almost half (n = 544, 46%) of those with Type II diabetes were diagnosed with DR.
Among those who were diagnosed with DR, 168 (31%) had mild DR, 309 (57%) had
moderate to severe DR, and 67 (12%) had proliferative DR (PDR).
Figure 1. Distribution of Diabetic Retinopathy in Type II Diabetics
Moderate-
Severe
26% ,
None
54%
PDR=Proliferate Diabetic
D o tin r tn o th \/
Table 1 shows the results of the risk factors and their univariate associations
with any DR. Candidate risk factors (p<0.10) for the multivariable analyses are
noted in the last column of the table. Age (p=0.02), gender and country of birth (both
p<0.10) were the socio-demographic variables found to be candidate risk factors
associated with DR. Those with DR were more likely to be older, male, and bom in
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the United States. For a more detailed distribution and associations across the
diabetic retinopathy disease spectrum, see Appendix B.
Healthcare utilization variables associated with any DR included number of
doctor visits in the past 12 months and time since last complete eye exam (both
p<0.05). Those with DR were less likely to have recent health care or eye
examinations.
Clinical features associated with any DR included BMI, duration of diabetes,
blood glucose level, HbAlc, systolic and diastolic blood pressure and insulin use,
history of hypertension, systolic blood pressure (all p<0.01) and diastolic blood
pressure (p=0.08). Those participants with DR were less likely to be obese, more
likely to have a longer duration of diabetes, high blood glucose and HbAlc levels,
high blood pressure, and less likely to be on insulin. Ocular parameters associated
with DR included cataract surgery and refractive spherical equivalent (p<0.10). No
lifestyle factors were associated with any DR (p>0.10).
Risk Factors
Any Diabetic Retinopathy
p-value
Selected
Covariates+
None
(N=643)
Yes
(N-544)
n (%) n (%)
Sociodemographic Factors
Age Group (years)
40-49 (Index)
50-59
60-69
70-79
80+
160 24.9%
216 33.6%
172 26.8%
77 12.0%
18 2.8%
102 18.8%
178 32.7%
159 29.2%
93 17.1%
12 2.2%
0.02 X
Gender
Female (Index)
Male
375 58.3%
268 41.7%
288 52.9%
256 47.1%
0.06 X
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8
Table 1. Continued
Risk Factors
Any Diabetic Retinopathy
p-value
Selected
Covariates+
None
(N=643)
Yes
(N=544)
n (%) n (%)
Sociodemographic Factors
Country of Birth
US (Index)
Mexico
Other
181 28.2%
397 61.8%
64 10.0%
173 31.8%
334 61.4%
37 6.8%
0.09 X
Native American Ancestry
No (Index)
Yes
604 34.1%
38 5.9%
506 93.0%
38 7.0%
0.46
Acculturation
Low (Index)
High
401 62.5%
241 37.5%
350 64.3%
194 35.7%
0.50
Education Level
0-5(lndex)
6-11
12+
183 28.5%
258 40.2%
201 31.3%
178 32.7%
209 38.4%
157 28.9%
0.28
Income Level
<=$20,000 (Index)
>$20,000
218 53.8%
273 46.2%
254 51.6%
238 48.4%
0.47
Access to Healthcare
Health Insurance
None (Index)
Health Insurance
440 68.5%
202 31.5%
386 71.1%
157 28.9%
0.34
Vision Insurance
lndex=None
Vision Insurance
362 56.7%
277 43.4%
319 59.2%
220 40.8%
0.38
Visits to health care
provider in last 12 months
None (Index)
1 to 4
5 to 9
10+
76 11.8%
322 50.2%
111 17.3%
133 20.7%
58 10.7%
237 43.6%
103 18.9%
146 26.8%
0.04 X
Last Complete Eye Exam
Never (Index)
5+ years ago
3-5 years ago
1-3 years ago
Within 12 months
190 33.8%
43 7.7%
22 3.9%
157 27.9%
150 26.7%
118 24.8%
30 6.3%
26 5.5%
136 28.6%
166 34.9%
0.005 X
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9
Table 1. Continued
Risk Factors
Any Diabetic Retinopathy
p-value
Selected
Covariates+
None
(N=643)
Yes
(N=544)
n (%) n (%)
Clinical Factors
Body Mass Index
Less than 25 Kg/m2 (Index)
Overweight (25-29.9 Kg/m2)
Obese (>=30.0 Kg/m2)
39 6.1%
192 30.2%
404 63.6%
52 9.9%
196 37.5%
275 52.6%
0.0004 X
Waist/Hip Ratio
lndex=Low/Normal (Men)
High: Men>0.95
lndex=Low/Normal (Women)
High: Women >0.8
74 27.8%
192 72.2%
19 5.2%
349 94.8%
67 26.7%
184 73.3%
8 2.8%
277 97.2%
0.77
0.13
Duration of Diabetes (yrs)
Newly diagnosed (Index)
1-4
5 to 9
10 to 14
15+
190 29.6%
237 36.9%
97 15.1%
71 11.1%
47 7.3%
58 10.7%
90 16.5%
124 22.8%
106 19.4%
166 30.5%
<0.0001 X
Blood Glucose Level
<140mg% (Index)
140-200 mg%
>200 mg%
249 38.7%
163 25.4%
231 35.9%
139 25.6%
128 23.5%
277 50.9%
<0.0001 X
HbAlc
<6.5 (Index)
6.5-10
>10.0
127 19.8%
399 62.1%
117 18.2%
63 11.6%
336 61.8%
145 26.7%
<0.0001 X
Treatment
No Insulin (Index)
Insulin
66 10.3%
577 89.7%
138 25.4%
406 74.6%
<0.0001 X
Blood Pressure
Systolic BP (>140 mmHg)
Diastolic BP (>90 mmHg)
154 24.0%
59 9.2%
172 31.8%
67 12.4%
0.003
0.08
X
X
Lifestyle Factors
Alcohol
Never (Index)
Partial drinker
Regular drinker
261 40.7%
313 48.8%
68 10.6%
224 41.2%
281 51.7%
39 7.2%
0.11
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10
Table 1. Continued
Any Diabetic Retinopathy
Risk Factors
None
(N=643)
Yes
(N=544)
p-value
Selected
Covariates+
n
(%)
n (%)
Smoking
Never (Index) 374 58.4% 302 55.9%
0.66
Ex-smoker 186 29.1% 169 31.3%
Current smoker 80 12.5% 69 12.8%
Occular Parameters
Cataract Surgery (lndex=none)
IOL either eye 28 4.4% 50 9.2% 0.001 X
IOL both eyes 18 2.8% 34 6.3% 0.004 X
Aphakia either eye 3 0.5% 2 0.4% 0.80
Aphakia both eyes 0 0.0% 0 0.0%
Ref. Spherical equiv.
(Left eye)
<-3.0 Diopters 52 80.9% 24 4.4%
-3.0 to 0.50 D 113 17.6% 107 19.7% 0.08 X
-0.5 to +0.5 D (Index) 242 37.6% 219 40.3%
+0.5 to +3.0 D 211 32.8% 168 30.9%
>3.0 D 25 3.9% 26 4.8%
Ref. Spherical equiv.
(Right eye)
<-3.0 Diopters 50 7.8% 31 5.7%
-3.0 to 0.50 D 103 16.0% 114 21.0% 0.05 X
-0.5 to +0.5 D (Index) 261 40.6% 192 35.3%
+0.5 to +3.0 D 206 32.0% 180 33.1%
>3.0 D 23 3.6% 27 5.0%
+ = p-values of 0.1 or less entered in the multivariate logistic regression model
Table 2 presents the results of the forward stepwise logistic regression
analyses. The dependent variable was diabetic retinopathy; the independent
variables were all candidate risk factors identified in Tables 1 and 2. Duration of
diabetes was found to be the primary risk factor associated with any type of DR, with
those participants having diabetes for more than 15 years having a 12-fold increase
in the likelihood of DR compared to those who were newly diagnosed with diabetes
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11
(0R=11.92; 95% Cl = 7.19, 19.74; pO.OOOl). Those participants with blood glucose
levels greater than 200 mg% were almost twice as likely to have any DR compared
to those with blood glucose levels less than 140 mg% (OR=T.86; 95% Cl = 1.28,
2.72; p=0.0012). Participants with diastolic blood pressure greater than 90 mmHg
were almost twice as likely to have any DR compared to those participants who had
diastolic blood pressures below this level (OR=1.77; 95% Cl = 1.13, 2.77; p=0.013).
Those participants being treated with insulin were over 50% more likely to have any
DR compared to those not being treated with insulin (OR=1.58; 95% Cl = 1.06,
2.34;p=0.023). Males were more likely than females to have any DR (OR=1.37;
95% Cl = 1.03, 1.82; p = 0.03). Having HbAlc levels greater than 10% conferred
an almost two-fold risk of any DR compared to those participants who have HbAlc
levels less than 6.5% (OR=1.96; 95% Cl = 1.15, 3.34; p = 0.013).
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12
Table 2. Stepwise Multivariable Model of Diabetic Retinopathy
Risk Factor
Step in
Selection
Any DR vs No DR
OR (95% Cl) p-value
Diabetes Duration 1
Newly diagnosed (Index) 1.00
1-4 years 1.49 (0.97, 2.29) 0.06
5-9 years 4.45 (2.85, 6.96) <0.0001
10-14 years 4.63 (2.89, 7.43) <0.0001
15+ years 11.92(7.19, 19.74) <0.0001
Blood glucose levels 2
<140 (Index) 1.00
140-200mg% 1.09 (0.75, 1.60) 0.65
>200mg% 1.86(1.28, 2.72) 0.0012
Diastolic BP 3
<90 (Index) 1.00
>=90 1.77(1.13, 2.77) 0.013
Treatment
No Insulin (Index) 4 1.00
Insulin 1.58(1.06, 2.34) 0.023
Gender
Female (Index) 5 1.00
Male 1.37(1.03, 1.82) 0.03
HbAlc
<6.5 (Index) 6 1.00
6.5-10 1.62 (1.07, 2.46) 0.02
>10 1.96(1.15, 3.34) 0.013
When comparing those who were diagnosed with PDR to those others who
had NPDR, insulin, systolic blood pressure, and time since last complete eye exam
were found to be risk factors for PDR (Table 3). Those diabetic patients who were
on insulin alone were almost four times more likely to have PDR compared to those
taking oral hypoglycemic medications or diet alone (OR=3.91; 95% CI=2.04-7.48;
p<0.0001). High systolic blood pressure greater than 140 mmHg increased the risk
of PDR 3-fold compared to systolic blood pressure below this level (OR=2.71; 95%
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13
0=1.42-5.18; p=0.003). Those participants who had completed an eye exam within
the last twelve months were almost four times more likely to be diagnosed with PDR
compared to those who have never had an eye exam (OR=3.95; 95% 0=1.55-10.07;
p=0.004).
Table 3. Stepwise Multivariable Model of Proliferate Diabetic Retinopathy
Step in
PDR vs Non-PDR
Risk Factor Selection
OR (95% Cl) p-value
Treatment 1
No Insulin (Index) 1.00
Insulin 3.77(1.99, 7.13) <0.0001
Systolic BP 2
<140 (Index) 1.00
>=140 2.89(1.53, 5.47) 0.001
Last complete eye exam 3
Never (Index) 1.00
3+ years ago 0.32 (0.04, 2.82) 0.31
<3 years ago 2.89(1.53, 5.47) 0.04
Logistic regression analyses were also conducted using a backward stepwise
procedure. All candidate risk factors were entered into the model, and eliminated
based on lack of significance. Similar results were obtained as those found using the
forward stepwise procedure.
Stratified Analyses Evaluating Sociodemographic Characteristics on Increases
in the Risk of DR: In evaluating the impact of sociodemographic factors (gender,
income, education, and Native-American ancestry), the following relationships were
observed. Stratified analyses by gender indicated that having a blood glucose level
greater than 200mg% increased the risk of DR in females by 2.3 times that of those
with a blood glucose level less than 140 mg% (OR: 2.34; 95% Cl: 1.72-3.19), while
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14
males had a 1.4 times increase in the risk of DR (OR: 1.36; 95% Cl: 0.96-1.93);
p=0.02, Breslow-Day test for homogeneity.
Stratified analyses by Native-American ancestry indicated that the risk of DR
for Native-Americans having a duration of diabetes>10 years was greater that that
for participants who did not report a Native American ancestry (OR: 23.33, p<0.0001
vs. 4.35, p<0.0001), p=0.01. No other sociodemographic characteristics were
identified.
Stratified Analyses Evaluating the Impact of Modifiable Variables on the Risk
of DR: In evaluating the modifiable variables (smoking, alcohol, and obesity), the
following relationships were observed. The risk of DR among patients who have
uncontrolled HbAlc levels greater than 7.0% is greater in current smokers
(OR=4.86; p<0.001) than never smokers (OR=2.06; p<0.001) or ex-smokers
(OR=1.44; p=0.12), respectively (p=0.06, Breslow-Day test for homogeneity of the
odds ratios). Blood glucose levels show similar results, namely, those patients who
have a blood glucose level greater than 200mg% are at a much greater risk of DR if
they are current smokers (OR=3.85, p <0.0001) compared to ex-smokers (OR=1.54,
p=0.049) and never smokers (OR=T.74; p<0.001), respectively (p=0.06).
In our stratified analyses by obesity, we found that having blood glucose
levels greater than 200mg% and being obese increased the risk of DR compared to
those who were not obese, OR=2.23 (p<0.0001) vs. 1.47 (p=0.04), respectively
(p=0.04, one-tailed test). In addition, the risk of DR for participants who had
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15
diabetes for more than 10 years was greater in participants who were obese (OR =
5.65, p<0.0001) as compared to those who were not obese (OR = 3.61, p<0.0001),
p<0.05, one-tailed test). Obesity also increased the risk of DR in those participants
who were on insulin treatment. The risk of DR was greater for those participants on
insulin who were obese (OR=1.97; p<0.0001) compared to those participants on
insulin who were not obese (OR=T.41; p<0.001), p=0.03, one-tailed test.
No significant differences were found for alcohol.
DISCUSSION
Summary of Findings. Socio-demographic and clinical risk factors were found to
be associated with the presence of DR in this population-based cohort of Latinos
aged 40 and older. In the stepwise analysis for any DR compared with no DR,
duration of diabetes, blood glucose level, diastolic blood pressure, insulin treatment,
male gender and HbAlc were statistically significant independent risk indicators.
These socio-demographic and clinical factors have previously been identified as risk
1 T 9 0 9 4
indicators associated with DR in Latinos and in non-Hispanic whites. ’
In the stepwise analysis for PDR compared with non-PDR, insulin treatment,
systolic blood pressure and recent eye examinations were statistically significantly
associated with retinopathy. Duration of diabetes and HbAlc, which are factors
associated with the chronicity of diabetes and were identified as risk indicators of
DR, were not related to PDR. This finding implies that once significant damage to
the microvascular retina has occurred, duration of diabetes and glycemic levels are
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16
no longer relevant. This could be explained by the hyperglycemic memory in which
there is a progression and persistence of the microvascular damage caused by the
hyperglycemic status, even during periods of normal levels of glycemia.
The association with high blood pressure indicates that damage of the
microvascular retina is aggravated in PDR. The finding that insulin treatment is
associated with more advanced retinopathy, suggests that this more aggressive
treatment is necessary during the ultimate phase of the disease.
Having an eye exam within the last 12 months could indicate a higher use of
health care services once the vision decreased as a result of the retinopathy
complication. We perceive that the more frequent use of a health care service is
associated when the retinopathy reaches an advanced status.
Comparison with Other Studies. We did not find a risk factor relation of
DR with low BMI or low income, as reported in a previous study in Mexican-
Americans.1 5 However, stratified analyses found that obesity was a significant
moderating factor that increased the risk of DR. Our finding that diastolic blood
pressure was associated with any DR and PDR, after adjusting for blood glucose
level and insulin treatment, was similar to that reported in the WESDR,2 9 but
contrary to the association with high systolic blood pressure found in the UKPDS.
Thus, high diastolic blood pressure can be considered a significant risk factor for DR
and more consistent than systolic blood pressure, although a study in a white
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17
population found both high systolic and diastolic blood pressure associated with
I 'j
diabetic retinopathy.
In our stepwise regression analyses, there was no association with alcohol or
cigarette smoking as has been found in other reports.2 6 '3 0 However, stratified
analyses found that current cigarette smoking to be a significant moderating factor
that increased the risk of DR.
Study Limitations. We consider that our results are limited to the variables studied,
and further studies are needed to evaluate the association of DR with lipoprotein
levels, nutritional habits, antioxidants supplementation and other factors associated
with retinopathy such as protein kinase C.
Conclusions. Our study showed that the increased risk of diabetic retinopathy in
adult Latinos is due to several risk factors that have been associated among the Non-
Hispanic White and African-American populations, and risk was increased by
several modifiable factors. The prevalence of diabetes and diabetic retinopathy has
been reported to be greater in Latinos than in non-Hispanic Whites and African-
Americans, and this excess does not appear to be due to a greater susceptibility to the
known risk factors. Thus, other mechanisms such as those related with biochemical
processes (increased polyol pathway, increased glycation end-product formation,
activation of protein kinase C, and increased hexosamine pathway flux) as well as
genetic-associated factors should be investigated to understand the observed greater
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18
rates of DR in Latinos. In order to quantify and better understand the strength of
these variables as risk factors further longitudinal studies will be necessary.
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19
REFERENCES
(Alphabetized)
19. Early photocoagulation for diabetic retinopathy: ETDRS report number 9. Early
Treatment Diabetic Retinopathy Study Research Group. Ophthalmology.
1991;98:766-785.
28. Brown JB, Pedula KL, Summers KH. Diabetic retinopathy. Contemporary
prevalence in a well-controlled population. Diabetes Care 2003;26:2637-2642.
25. Brownlee M. Biochemestry and molecular cell byology of diabetic
complications. Nature 414:13;813-20 2001.
21. Haffner SM, Fong D, Stem MP, Pugh JA, Hazuda, Patterson JK, VanHeuven
WAJ, Klein R. Diabetic retinopathy in Mexican Americans and non-Hispanic whites.
Diabetes 37:878-84,1988.
17. Hamman RF, Mayer EJ, Moo-Young GA, Hildebrandt W, Marshall JA, Baxter J.
Prevalence and risk factors of Diabetic Retinopathy in Non-Hispanic Whites and
Hispanics With NIDDM. San Luis Valley Diabetes Study. Diabetes. 1989;38:231-
237.
9. Hanis C, Hewett-Emmett D, Bertin T, Schull W. Origins of US Hispanics,
Implications for diabetes. Diabetes Care 1991;14 (7 Suppl 3):618-27.
8. Harris M. Epidemiological correlates of NIDDM in Hispanics, Whites and Blacks
in the US population. Diabtes Care 1991;14 (Suppl. 3):639-48.
10. Harris M, Klein R, Cowie CC, Rowland M, Byrd-Holt DD. Is the risk of diabetic
retinopathy greater in non-hispanic blacks and Mexican-americans than in non-
hispanic whites with type 2 diabetes? Diabetes Care 1998;21:1230-1235.
2. Isomaa B, Henriesson M, Almgren P, Tuomi T, Taskinen M-R, Groop L. The
metabolic syndrome influences the risk of chronic complications in patients with
type II diabetes. Diabetologia 2001 ;44:1148-1154.
5. Keen H, Lee ET, Russell D, Miki E, Bennett PH, Lu M. The appearance of
retinopathy and progression to proliferative retinopathy: The WHO multinational
study of vascular disease in diabetes. Diabetologia 2001;44(Suppl 2): S22-S30.
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22. Keen H, Lee ET, Russell D, Miki E, Bennet PH, Lu M and the WHO
Multinational Study Group. Diabetologia 44 suppl2:S22-30 2001.
30. Klein BE, Davis MD, Segal P, Long JA, Harris WA, Haug GA, Magli YL,
Syijala S. Diabetic retinopathy assesment of severity and progression. Opthalmology
91:10-17 1984.
3. Klein R, Marino EK, Kuller LH, Polak JF, Tracy RP, Gottdiener JS, Burke GL,
Hubbard LD, Boineasu R. The relation of atherosclerotic cardiovascular disease to
retinopathy in people with diabetes in the Cardiovascular Health Study. Br J
Ophthalmol 2002;86:84-90.
12. Klein R, Klein BEK. Blood pressure control and diabetic retinopathy. Br J
Ophthalmol 2002;86:365-367.
27. Klein R. Prevention of visual loss from diabetic retinopathy. Surv Ophthalmol 47
suppl2:S246-S252 2002.
29. Klein R, Klein BE, Moss SE, Cruickshanks KJ. The Wisconsin Epidemiologic
Study of diabetic retinopathy. XIV. Ten-year incidence and progression of diabetic
retinopathy. Arch Ophthalmol 112:1217-28 1994.
6. Porta M, Sjoelie A-K, Chaturvedi N, Stevens L, Rottiers R, Veglio M, Fuller JH.
Risk factors for progression to proliferative diabetic retinopathy in the EURODIAB
Prospective Complications Study. Diabetologia 2001;44:2203-2209.
20. Service FJ, O’Brien PC. The relation of glycaemia to the risk of development and
progression of retinopathy in the Diabetic Control and Complications trial.
Diabetologia 2001;44:1215-1220.
4. Stem MP, Rosenthal M, Haffher SM, Hazuda HP, Franco LJ. Sex difference in the
effects of sociocultural status on diabetes and cardiovascular risks factors in Mexican
Americans. Am J ophthal 1984;120:834-851.
14. Stem MP, Gaskill SP, Hazuda HP, Gardner LI, Haffher SM. Does obesity
explain the excess prevalence of diabetes among Mexican-Americans? Diabetologia
1983;24:272-277.
24. Stem MP, Haffher SM. Type II Diabetes and its complications in Mexican
americans. Diab/Met Rev 6:l;29-45 1990.
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7. Stratton IM, Mohner Em, Aldington SJ, Turner RC, Holman RR, Manley SE,
Matthews DR. UKPDS 50: Risk factors for incidence and progression of retinopathy
in type II diabetes over 6 years from diagnosis. Diabetologia 2001;44:156-163.
23. Stratton IM, Kohner EM, Aldington SJ, Turner RC, Holman RR, Manley SE,
Matthews DR for the UKPDS Group. Diabetologia 44:156-163 2001.
18. Tudor SM, Hamman RF, Baron A, Johnson DW, Shetterly S. Incidence And
Progression Of Diabetic Retinopathy In Hispanics And Non-Hispanic Whites With
Type 2 Diabetes. San Luis Valley Diabetes Study, Colorado. Diabetes Care.
1998;21:53-61.
13. Van Leiden HA, Dekker JM, Moll AC, Nijpels G, Heine RJ, Bouter LM,
Stehouwer CDA, Polak BCP. Blood pressure, lipids and obesity are associated with
retinopathy. Diabetes Care 2002;25:1320-1325.
11. Varma R, Torres M, Pena F, et al. Prevalence of Diabetic Retinopathy in Adult
Latinos: The Los Angeles Latino Eye Study. Ophthalmology [In press].
16. Varma R, Paz S, Azen S, et al. The Los Angeles Latino Eye Study: Design,
Methods and Baseline Data. Ophthalmology 111:1122-32,2004.
26. West KM, Erdreich LJ, Stober JA. A detailed study of risk factors for retinopathy
and nephropathy in diabetes. Diabetes 29:501-508 1980.
15. West SK, Munoz B, Klein R, Broman AT, Sanchez R, Rodriguez J, Snyder R.
Risk factors for type II diabetes and diabetic retinopathy in a Mexican-American
Population: Proyecto VER. Am J Ophthalmol 2002;134:390-398.
1. Zimmet P, Alberti K, Shaw J. Global and societal implications of the diabetes
epidemic. Nature 414:782-787.
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22
APPENDIX A
The Los Angeles Latino Eye Study Group
University of Southern California
Rohit Varma MD, MPH (Principal Investigator); Sylvia H. Paz MS (Project
Director); LaVina Abbott, Stanley P. Azen PhD (Co-Principal Investigator), Lupe
Cisneros COA, Elizabeth Corona, Carolina Cuestas OD, Denise R Globe PhD, Sora
Hahn MD, Mei Lai MS, George Martinez, Susan Preston- Martin PhD, Ronald E.
Smith MD, Mina Torres MS, Natalia Uribe OD, Joanne Wu MPH, Myma Zuniga,
Fernando Pena MD.
Battelle Survey Research Center
Sonia Chico, Lisa John MSW, Michael Preciado, Karen Tucker MA.
University of Wisconsin
Ronald Klein MD, MPH; S. Tiffany Jan, BA; Stacy M. Meuer, BS; Scot E. Moss,
MA; Michael W. Neider, BA; Sandra C. Tomany, MS.
LALES External Advisory Committee who gave their advice and contributions: Roy
Beck, MD, PhD, (Chairman) Natalie Kurinij, PhD, Leon Ellwein, PhD, Helen
Hazuda, PhD, Eve Higginbotham, MD, Lee Jampol, MD, M. Cristina Leske, MD,
Donald Patrick, PhD, and James M. Tielsch, PhD.
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23
APPENDIX B
Distribution of Risk Factors Across Diabetic Retinopathy Disease Spectrum
Risk Factors
Diabetic Retinopathy
p-value None
(N=643)
Non-PDR
(N=477)
PDR
(N*67)
n
(% >
n
(%)
n (%)
Sociodemographic Factors
Age Group (years)
40-49 (Index) 160 24.9% 93 19.5% 9 13.4% 0.04
50-59 216 33.6% 160 33.5% 18 26.9%
60-69 172 26.8% 134 28.1% 25 37.3%
70-79 77 11.9% 79 16.6% 14 20.9%
80+ 18 2.8% 11 2.3% 1 1.5%
Gender
Female (Index) 375 58.3% 248 52.0% 40 59.7% 0.09
Male 268 41.7% 229 48.0% 27 40.3%
Country of Birth
US (Index) 181 28.2% 151 31.7% 22 32.8% 0.25
Mexico 397 61.8% 295 61.8% 39 58.2%
Other 64 9.9% 31 6.5% 6 8.9%
Native American Ancestry
No (Index) 604 34.1% 446 93.5% 60 89.6% 0.35
Yes 38 5.9% 31 6.5% 7 10.5%
Acculturation
Low (Index) 401 62.5% 309 64.8% 41 61.5% 0.67
High 241 37.5% 168 35.2% 26 38.8%
Education Level
Q-5(lndex) 183 28.5% 155 32.5% 23 34.3% 0.56
6-11 258 40.2% 182 38.0% 27 40.3%
12+ 201 31.3% 140 29.4% 17 25.4%
Income Level
<=$20,000 (Index) 318 53.8% 220 50.9% 34 56.7% 0.55
>$20,000 273 46.2% 212 49.1% 26 43.3%
Healthcare Utilization
Health Insurance
None (Index) 202 31.5% 146 30.7% 11 16.4% 0.04
Health Insurance 440 68.5% 330 69.3% 56 83.6%
Vision Insurance
lndex=None 277 43.4% 202 42.8% 18 26.9% 0.03
Vision Insurance 362 56.7% 270 57.2% 49 73.1%
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24
APPENDIX B
(continued)
Diabetic Retinopathy
Risk Factors
None
(N=643)
Non-PDR
(N=477)
PDR
(N=67)
p-value
n <% ) n
(%)
n
(%)
Visits to health care provider in
last 12 months
None (Index) 76 11.8% 52 10.9% 6 8.9% 0.0003
1 to 4 322 50.2% 222 46.5% 15 22.4%
5 to 9 111 17.3% 85 17.8% 18 26.9%
10+ 133 20.7% 118 24.7% 28 41.8%
Last Complete Eye Exam
Never (Index) 190 33.8% 111 26.1% 7 14.0% <0.0001
5+ years ago 43 7.7% 30 7.0% 0 0.0%
3-5 years ago 22 3.9% 25 5.9% 1 2.0%
1-3 years ago 157 27.9% 127 29.8% 9 18.0%
Within 12 months 150 26.7% 133 31.2% 33 66.0%
Clinical Factors
Body Mass Index
Less than 25 Kg/m2 (Index) 39 6.1% 42 9.1% 10 15.9% 0.0003
Overweight (25-29.9 Kg/m2) 192 30.2% 169 36.7% 27 42.9%
Obese (>=30.0 Kg/m2) 404 63.6% 249 54.1% 26 41.3%
Waist/Hip Ratio
lndex=Low/Normal (Men) 74 27.8% 59 26.2% 8 30.8% 0.85
High: Men>0.95 192 72.2% 166 73.8% 18 69.2%
lndex=Low/Normal (Women) 19 5.2% 8 3.3% 0 0.0% 0.2
High: Women >0.8 349 994.8% 237 96.7% 40 100.0%
Blood Glucose Level
<140mg% (Index) 249 38.7% 122 25.6% 17 25.4% <0.0001
140-200 mg% 163 25.4% 112 23.5% 16 23.9%
>200 mg% 231 33.9% 243 50.9% 34 50.8%
Duration of Diabetes (yrs)
Newly diagnosed (Index) 190 29.6% 56 11.7% 2 3.0% <0.0001
1-4 237 36.9% 87 18.2% 3 4.5%
5 to 9 97 15.1% 113 23.7% 11 16.4%
10 to 14 71 11.1% 92 19.3% 14 20.9%
15+ 47 7.3% 129 27.0% 37 55.2%
HbA1c
<6.5 (Index) 127 19.8% 53 11.1% 10 14.9% <0.0001
6.5-10 399 62.1% 291 61.0% 45 67.2%
>10.0 117 18.2% 133 27.9% 12 17.9%
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25
APPENDIX B
(continued)
Diabetic Retinopathy
Risk Factors
None
(N=643)
Non-PDR
(N=477)
PDR
(N=67)
p-value
n
(%)
n
(%)
n
(%)
Treatment
No Insulin (Index) 577 89.7% 373 78.2% 33 49.3% <0.0001
Insulin 66 10.3% 104 21.8% 34 50.8%
Blood Pressure
Systolic BP (>140 mmHg) 154 23.9% 143 30.2% 29 43.3% 0.0009
Diastolic BP (>90 mmHg) 59 9.2% 56 11.8% 11 16.4% 0.11
Lifestyle Factors
Alcohol
Never (Index) 261 40.7% 193 40.5% 31 46.3% 0.27
Partial drinker 313 48.8% 249 52.2% 32 47.8%
Regular drinker 68 10.6% 35 7.3% 4 6.0%
Smoking
Never (Index) 374 58.4% 262 55.4% 40 59.7% 0.85
Ex-smoker 186 29.1% 149 31.5% 20 29.9%
Current smoker 80 12.5% 62 13.1% 7 10.5%
Occular Assessments
Cataract Surgery (lndex=none)
IOL either eye 28 4.4% 35 7.4% 15 22.4% <0.0001
IOL both eyes 18 2.8% 26 5.5% 8 11.9% 0.0008
Aphakia either eye 3 0.5% 1 0.2% 1 1.5% 0.31
Aphakia both eyes 0 0.0% 0 0.0% 0 0.0% NA
Ref. Spherical equiv. (Left eye)
<-3.0 Diopters (Index) 52 8.1% 21 4.4% 3 4.5% 0.11
-3.0 to 0.50 D 113 17.6% 88 18.5% 19 28.4%
-0.5 to +0.5 D 242 37.6% 198 41.5% 21 31.3%
+0.5 to +3.0 D 211 32.8% 147 30.8% 21 31.3%
>3.0 D 25 3.9% 23 4.8% 3 4.5%
Ref. Spherical equiv. (Right eye)
<-3.0 Diopters (Index) 50 7.8% 25 5.2% 6 9.0% 0.1
-3.0 to 0.50 D 103 16.0% 100 21.0% 14 20.9%
-0.5 to +0.5 D 261 40.6% 174 36.5% 18 26.9%
+0.5 to +3.0 D 206 32.0% 156 32.7% 24 35.8%
>3.0 D 23 3.6% 22 4.6% 5 7.5%
PDR: Proliferative Diabetic Retinopathy
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Risk factors for diabetic retinopathy in Latinos: Los Angeles Latino eye study
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