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Original Article
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Risk factors for diabetic retinopathy in selfreported rural population with diabetes
Rani PK, Raman R, Chandrakantan A, Pal SS, Perumal GM, Sharma T
Vision Research
Foundation, Sankara
Nethralaya Diabetic
Retinopathy Project, 18,
College Road,
Sankara Nethralaya,
Chennai – 600 006,
Tamil Nadu, India
Address for correspondence:
Dr. Tarun Sharma,
E-mail: [email protected]
Received
: 15-04-08
Review completed : 17-01-09
Accepted
: 24-02-09
PubMed ID
: ????
DOI: 10.4103/0022-3859.48787
J Postgrad Med 2009;55:92-6
ABSTRACT
Background: Diabetes and its related microvascular complications like diabetic retinopathy (DR) are showing
increased prevalence in India. However, the magnitude of DR in rural population with diabetes needs exploration.
Aim: To estimate the prevalence and risk factors for the presence and severity of diabetic retinopathy in
the self-reported rural population with diabetes. Settings and Design: In a cross-sectional study, a total of
26,519 participants (age ≥ 30 years) attended 198 diabetic retinopathy screening camps conducted in three
southern districts of Tamilnadu, India, between February 2004 and April 2006. Materials and Methods: All
the participants underwent a dilated eye examination to detect DR by indirect ophthalmoscopy. Systemic
and ocular risk factor estimation was done in a comprehensive examination. Statistical Analysis: Univariate
and stepwise regression analyses were done to identify the independent risk factors associated with the
presence and severity of retinopathy. Results: The prevalence of diabetic retinopathy was 17.6% among the
self-reported rural population with diabetes. The prevalence of referable (sight threatening) retinopathy was
5.3%. Risk factors associated with the development of any DR were male gender (OR= 1.37), longer duration
of diabetes (per year, OR= 1.07), lean body mass index (OR= 1.30), higher systolic blood pressure (per
10 mm Hg, OR= 1.18), and insulin treatment (OR= 1.34; P < 0.0001). Risk factors associated with referable
retinopathy included longer duration of diabetes (per year, OR= 1.22), lean body mass index (OR= 1.25),
higher systolic blood pressure (per 10 mm Hg, OR= 1.03), and insulin treatment (OR= 1.36; P < 0.0001).
Conclusion: The study identified risk factors associated with DR in the rural population with diabetes. The
results suggested that there was a need for formulating effective preventive strategies to minimize avoidable
blindness due to diabetes, in rural areas.
KEY WORDS: Diabetic retinopathy, ocular risk factors, rural population, systemic risk factors
D
iabetic Retinopathy (DR), a microvascular complication,
develops in nearly all persons with type 1 diabetes and
in more than 77% of those with type 2 diabetes, who survive
for over 20 years with the disease.[1] The burden of diabetes is
reaching an alarming proportion in India. The World Health
Organization (WHO) estimates an increase in population
with diabetes: from 30 million in 2000 to 80 million in 2030.[1]
WHO also estimates that DR is responsible for 4.8% of
the 37 million cases of blindness throughout the world.[2]
and associated risk factors in a self-reported cohort of persons
with diabetes attending diabetic retinopathy screening camps
in rural areas.
Materials and Methods
Earlier, diabetes mellitus (DM) was considered an urban disease.
However, recent studies (population-based and self-reported)
have shown an increasing prevalence in rural areas as well.[3-5]
Ramachandran et al.,[4] showed nearly a three-fold increase
in the rural prevalence of diabetes to 6.3% in 2003 compared
to 2.2% in 1989. In a cross-sectional study of a self-reported
population attending diabetic retinopathy screening camps in
2006, in rural areas, we found the prevalence of diabetes as 20%
and that of diabetic retinopathy as 18%.[5]
Between February 2004 and April 2006, 198 diabetic retinopathy
screening camps were conducted in a cross-sectional study in
three southern districts of Tamilnadu. The methodology of
diabetic retinopathy screening camps is described in detail
elsewhere.[6] Various measures (such as organizing awareness
meetings in the community, focusing on diabetes and related
complications; displaying education materials such as leaflets,
banners or posters; and involving local diabetologists and
volunteers from NGOs such as Lions club) were employed
to maximize the effectiveness of these screening camps. The
procedures followed were in accordance with the Helsinki
Declaration of 1975, as revised in 2000. The Institutional Review
Board approved the study.
The aim of this study was to estimate the prevalence of DR
A target population with diabetes, aged 30 years and above,
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Rani, et al.: Risk factors for DR in rural population 
underwent a comprehensive dilated eye examination for the
diagnosis of diabetic retinopathy. Procedures adopted for the
diagnosis of diabetes mellitus and diabetic retinopathy, and data
collection for risk assessments are described below.
Diagnosis of diabetes mellitus
A patient was considered to be known diabetic, if there was
a referral letter from a diabetologist or if he/she was on an
antidiabetic medication. A person was considered to be a newly
diagnosed individual with diabetes, if the duration of diabetes
was less than a month.[5,8]
Diagnosis of diabetic retinopathy
The binocular indirect ophthalmoscope (Keeler Instruments
Inc. PA, USA) and a +20 D lens (Nikon) were used to examine
the fundus. Diabetic retinopathy was clinically graded by
an experienced retinal specialist as per the norms of the
International Clinical Diabetic Retinopathy and Diabetic
Macular Edema guidelines. [7] Non-referral retinopathy
included cases of mild and moderate, nonproliferative diabetic
retinopathy. Sight threatening diabetic retinopathy (Referable
diabetic retinopathy) was defined as severe nonproliferative
diabetic retinopathy (NPDR), proliferative diabetic retinopathy
(PDR), and clinically significant macular edema (CSME).[8]
Risk factor assessment
Risk factor analysis for diabetic retinopathy included the
following demographic, clinical, and ocular factors. The
demographic risk factors studied were age, gender, and family
income. The systemic risk factors studied included duration
of diabetes mellitus, physical activity status, alcohol intake,
smoking habits, family history of diabetes mellitus, neuropathy
and nephropathy history (tingling, numbness, foot ulcers, and
amputated toe/foot), and diabetic treatment. All subjects
underwent measurement of height and weight, after which
the body mass index (BMI) was calculated using the formula:
weight (kg) / height2 (m2).
Based on the BMI, individuals were classified as lean (male <20,
female <19), normal (male 20 – 25, female 19 – 24), overweight
(male 25 – 30, female 24 – 29) or obese (male >30, female
>29).[9] Blood pressure was measured with a sphygmomanometer,
with the patient in the sitting position. The ocular risk factors
included details of first and last eye examinations, any visual
complaint or history of laser or eye surgery. LogMAR charts were
used to assess the visual acuity.
Statistical analysis
SPSS (version 9.0) was used for statistical analysis. Prevalence
was expressed in percentages with a 95% confidence interval.
Tests of significance such as chi-square, t-tests, and Z tests
were applied appropriately. Univariate and stepwise logistic
regression analyses were performed to elucidate the risk factors
influencing the presence and severity of DR. The method of
variable selection was forward selection; this was started with
an empty model. The variable with the smallest p value, when
it was the only predictor in the regression equation, was placed
in the model. In each subsequent step, variables (one at a time)
with the smallest P value were added to the model or equation.
A p value of less than 0.05 was considered statistically significant.
Results
A total of 26,519 persons with diabetes participated in the 198
diabetic retinopathy screening camps.
Estimation of prevalence of diabetic retinopathy
Of the 26519 individuals with diabetes, persons with known
diabetes were 25860 (97.5%), and newly detected, 659 (2.5%)
[Table 1]. The prevalence of diabetic retinopathy was 4671/
26519 (17.6%). It was 4604 / 25860 (17.8%) in persons with
known diabetes and 67 / 659 (10.2%) in persons with newly
detected diabetes. Of the 4604 cases with diabetic retinopathy
in persons with known diabetes, 1390 (30.2%) were of referable
DR. Of the 67 cases with diabetic retinopathy in newly detected
diabetic retinopathy, 17 (25.4%) belonged to the referable DR
category. Prevalence of referable DR was more in persons with
known diabetes than in persons with newly diagnosed diabetes
(P <0.0001).
Assessment of demographic, systemic, and ocular risk factors
Tables 2 and 3 show the univariate analysis of various risk factors
associated with the presence and severity of diabetic retinopathy.
Factors associated (P <0.05) with the presence and severity of
diabetic retinopathy included increasing age, longer duration
of diabetes, insulin intake, lean individuals, higher systolic
and diastolic blood pressure, moderate visual impairment,
and cataract surgery. Male patients were associated more with
any diabetic retinopathy, but not with severity of diabetic
retinopathy. Change in intraocular pressure did not influence
the presence and severity of diabetic retinopathy.
Tables 4 and 5 present the results of stepwise forward and
backward, logistic regression analyses. All variables that
were significant in the univariate analyses were entered in a
multivariate model. The risk factors independently associated
with any diabetic retinopathy, [Table 4] in order of importance,
were, longer duration of diabetes, lean BMI, elevated systolic
Table 1: Diabetic retinopathy prevalence data
Prevalence of DR
Non-referable retinopathy# Referable retinopathy##
Persons with known diabetes n = 25860 [n (%) (95% CI)]
Persons with newly diagnosed
diabetes n = 659 [n (%) (95% CI)]
4604/25860 (17.80) (17.33 - 18.26)
3214/4604 (69.81) (68.48 - 71.13)
1390/4604 (30.19) (28.86 - 31.51)
67/659 (10.16) (7.85 - 12.46)
50/67 (74.63) (64.21 - 85.04)
17/67 (25.37) (15.04 - 35.91)
Pooled data n = 26519
[n (%) (95% CI)]
4671/26519 (17.61) (17.15 - 18.06)
3264/26519 (12.30) (11.90 - 12.69)
1407/26519 (5.30) (5.03 - 5.56)
Non-referable retinopathy# included cases of mild and moderate nonproliferative diabetic retinopathy, Referable retinopathy## included cases of severe
nonproliferative diabetic retinopathy, proliferative diabetic retinopathy and clinically significant macular edema; CI - Confidence interval ; DR - Diabetic
retinopathy
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Rani, et al.: Risk factors for DR in rural population
Table 2: Univariate analysis of risk factors associated with
presence of diabetic retinopathy
Variables
P*
No DR Any DR
(n-21848) (n-4671)
Table 3: Univariate analysis of risk factors associated with
severity of diabetic retinopathy
Variables
Non-referable Referable
DR (n-3264) DR (n-1407)
P
Demographic risk factors n %
n%
Age group (years)
Mean (±SD)
53.72 (10.88) 56.55 (9.48) <0.0001
30-39 (Index)
2012 (9.20)
169 (3.62)
40-49
5674 (25.97) 846 (18.11)
50-59
7115 (32.56) 1741 (37.27) <0.0001
>60
7047 (32.25) 1915 (41.00)
Gender
Female (Index)
11612 (53.14) 2088 (44.70)
Male
10236 (46.85) 2583 (55.29) <0.0001
Systemic risk factors
Duration of DM (years)
Mean (±SD) 4.89 (4.79) 8.58 (6.51) <0.0001
0-0.1 (Index)
592 (2.70)
67 (1.43)
0.1-4.9 12083 (55.30) 1378 (10.23)
5.0-9.9 5617 (25.70) 1255 (26.86)
>10
3556 (16.27) 1971 (42.19) <0.0001
Insulin No insulin (Index)
20576 (94.17) 4083 (87.41)
Insulin taken
1272 (5.82)
588 (12.58) <0.0001
BMI1
Lean
3089 (14.13) 1006 (21.53) <0.0001
Normal 10397 (47.58) 2471 (52.90)
Overweight
6563 (30.03) 1016 (21.75)
Obese (Index)
1799 (8.23)
178 (3.81)
Blood pressure
Mean SBP2 (±SD)
129.38 (18.27) 134.07 (20.10) <0.0001
>140 mm of Hg 6441 (29.48) 1847 (39.64) <0.0001
Mean DBP3 (±SD)
81.84 (10.42) 83.25 (11.19) <0.0001
>90 mm of Hg
6355 (29.08) 1574 (33.69) <0.0001
Ocular risk factors4
Visual impairment5
Mild 18565 (82.95) 3149 (77.54)
Moderate 2212 (9.88)
602 (14.82) <0.0001
Severe
1602 (7.15)
310 (7.63)
Cataract surgery
No (Index)
19228 (86.67) 3292 (84.43)
Yes
2957 (13.32) 607 (15.56)
0.0002
IOP
Mean (±SD) 16.31 (3.90) 16.06 (3.61) <0.0001
<21 mm of Hg (Index)
21453 (84.56) 856 (86.29)
>21 mm of Hg 3915 (15.43) 136 (13.70)
0.055
Demographic risk factors n (%)
n (%)
Age group (years) Mean (±SD)
56.27 (9.78) 57.20 (8.74) 0.0021
30-39 (Index)
138 (4.22)
31 (2.20)
40-49
629 (19.27) 217 (15.42)
50-59
1195 (36.61) 546 (38.80) <0.0001
60-69
1302 (39.88) 613 (43.56)
Gender
Female (Index)
1483 (45.43) 802 (57.00)
Male
1781 (54.56) 605 (42.99)
0.125
Systemic risk factors Duration of DM (years)
Mean (±SD)
8.01 (6.24) 9.90 (6.91) <0.0001
0-0.1 (Index)
5 (1.53)
17 (1.20)
0.1-4.9 105 (32.29) 324 (23.02)
5.0-9.9 90 (27.57) 355 (25.23)
>10
126 (38.60) 711 (50.53) 0.0005
Insulin No insulin (Index)
366 (11.21) 222 (15.77)
Insulin taken
2898 (88.78) 1185 (84.22) <0.0001
BMI1
Lean
672 (20.58) 334 (23.73) <0.0001
Normal 171 (52.38) 761 (54.08)
Overweight
747 (22.28) 269 (19.11)
Obese (Index)
135 (4.13)
43 (3.05)
Blood pressure
Mean SBP2 (±SD)
132.83 (19.27)136.93 (21.65) <0.0001
>140 mm of Hg
1208 (37.00) 639 (45.41) <0.0001
Mean DBP3 (±SD)
82.83 (10.67) 84.24 (12.27) <0.0001
>90 mm of Hg
1050 (32.16) 524 (37.24) <0.0001
Ocular risk factors4
Visual impairment5
Mild
2642 (81.19) 871 (62.08) <0.0001
Moderate
357 (10.97) 308 (21.95)
Severe
255 (7.83)
224 (15.96)
Cataract surgery
No (Index)
2656 (82.81) 1067 (78.16)
Yes
551 (17.18) 298 (21.83) 0.0003
IOP
Mean (±SD)
16.10 (3.29) 15.96 (4.26)
0.22
<21 mm of Hg (Index) 3141 (96.82) 1347 (96.48)
>21 mm of Hg
103 (3.17)
49 (3.50) 0.618
1
BMI: lean (male<20, female<19), normal (male 20–25, female 19–24),
overweight (male 25–30, female 24–29) or obese (male>30, female>29);
2
SBP-Systolic blood pressure; 3DBP- Diastolic blood pressure; 4Right eye was
selected for estimation of ocular risk factors; 5Visual impairment was defined
with level of visual acuity in the better eye: Mild (6/6 – 6/12), Moderate
(6/18–6/60) and Severe (<6/60). All variables with P≤0.1 were entered
in the multivariate regression model.*Chi-square procedure
BMI: lean (male<20, female<19), normal (male 20–25, female
19–24), overweight (male 25–30, female 24–29) or obese (male>30,
female>29); 2SBP-Systolic blood pressure; 3DBP - Diastolic blood
pressure; 4Right eye was selected for estimation of ocular risk factors;
5
Visual impairment was defined with level of visual acuity in the better
eye: Mild (6/6–6/12), Moderate (6/18–6/60) and severe (<6/60).
All variables with P ≤ 0.1 were entered in the multivariate regression model
Table 4: Stepwise regression analysis of risk factors
associated with presence of diabetic retinopathy
Table 5: Stepwise regression analysis of risk factors
associated with severity of diabetic retinopathy
Risk factor
Risk factor
Step in selection
Step in
selection
Diabetes duration (per year)
Lean body mass index
SBP (per 10 mm of Hg)
Insulin users
Male gender
1
2
3
4
5
No DR vs. any DR
OR (95% CI)
P*
1.071 (1.065 - 1.071)
1.300 (1.273 - 1.328)
1.184 (1.153 - 1.215)
1.347 (1.302 - 1.393)
1.369 (1.322 - 1.415)
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
OR – Odds ratio, CI – Confidence interval; *Stepwise logistic regression
procedure
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1
Diabetes duration (per year)
SBP (per 10 mm of Hg)
Lean body mass index
Insulin users
1
2
3
4
Non-referable DR vs.
referable DR
OR (95% CI)
P*
1.220 (1.198 - 1.242)
1.037 (1.000 - 1.094)
1.259 (1.166 - 1.352)
1.367 (1.239 - 1.483)
<0.0001
<0.0001
<0.0001
<0.0001
OR – Odds ratio, CI – Confidence interval; *Stepwise logistic regression
procedure
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Rani, et al.: Risk factors for DR in rural population 
blood pressure, insulin intake, and male gender. Similarly, the
risk factors independently associated with severity of diabetic
retinopathy, [Table 5] in order of importance, were, longer
duration of diabetes, elevated systolic blood pressure, lean BMI,
and insulin intake.
Discussion
The prevalence of diabetic retinopathy in a self-reported cohort
of people with diabetes, in the rural population of India,
was 17.6%. Even newly diagnosed individuals with diabetes
(as defined in this study) showed evidence of ‘any diabetic
retinopathy’ — around 10% — , and one-fourth of them showed
‘referable retinopathy’ (severe NPDR, PDR, and/or CSME).
Logistic regression analysis revealed certain independent
risk factors associated with both the presence and severity of
diabetic retinopathy; they were, longer duration of diabetes,
lean BMI, elevated systolic blood pressure, and insulin intake,
in the present study of the rural population with diabetes. The
duration of diabetes, however, remained the strongest predictor
for any diabetic retinopathy and its severity. Moreover, such an
association has been observed by several other investigators as
well.[10-15] The association showed a linear trend for any diabetic
retinopathy and also for referable diabetic retinopathy. Increased
duration influencing the occurrence of diabetic retinopathy and
its severity was probably related to the magnitude or prolonged
exposure, or both, to hyperglycemia coupled with other risk
factors. While the duration of diabetes was an independent risk
factor, 10% of the individuals with newly diagnosed diabetes
did show diabetic retinopathy, suggesting that these patients
would have been undiagnosed or undetected; in other words,
the duration of diabetes and the exact duration of hyperglycemia
did not go hand in hand.
Male gender was observed to be associated with the presence of
any DR (1.37 times), but not its severity. Similar observations
were made by Pradeepa et al., in an urban Indian population and
in the Los Angeles Latino Eye Study.[10,11] The inverse relation
between BMI and diabetic retinopathy was also observed in the
Indian population-based studies and also by others.[13-15] This
could be due to the catabolic effect of the lack of insulin over
a long duration of hyperglycemia, resulting in lean individuals.
There are evidences that South Asians have abdominal obesity
despite normal body mass indices, the so called “Asian Indian
phenotype”; which may explain this paradox.[16]
Further, it is interesting to note that in Caucasians, high BMI
is observed in subjects with diabetes, but in Asian population,
subjects with diabetes are lean with low BMI.[17] This may be
linked to the fact that Asians with type 2 diabetes mellitus
show lesser insulin secretion, but greater insulin sensitivity, as
compared to Caucasian diabetic patients.[18,19]
Every increase in systolic blood pressure by 10 mm of Hg showed
a linear trend, around 1 – 1.2 times the risk of influencing the
presence and severity of diabetic retinopathy. Such a correlation
between systolic blood pressure and diabetic retinopathy was
also noted by others.[11] The association noted with insulin
J Postgrad Med April 2009 Vol 55 Issue 2
therapy could be because patients with retinopathy are
preferentially started on insulin by their physicians.
Retinopathy was positively associated with moderate visual
impairment (6/18 – 6/60). Similar risk association with
moderate visual impairment was observed in our earlier
study.[5] Retinopathy was positively associated with the history
of cataract surgery. Cataract surgery as a risk factor for DR was
also reported in the Los Angeles Latino Eye Study.[11]
The limitation of the present study was the self-reported
diabetic population and so the possibility of a selection bias.
Identified risk factors were based on just point estimation;
therefore, a causal relationship with diabetic retinopathy could
not be proved. Nevertheless, some of the factors like systolic
blood pressure could be modulated, thereby reducing the risk
of preventable blindness in susceptible populations. Another
limitation of the present study was DR grading that was based
on indirect ophthalmoscopy and not on fundus photography
grading. This could have resulted in the underestimation of
the prevalence of DR.
There is a paucity of published data regarding DR prevalence
as well as risk factor estimates of the rural population with
diabetes. The present study gives us an important measure of
the DR burden and associated risk factors in a large sample
size of over 25000 individuals with diabetes, in rural settings.
Therefore, there is an urgent need to formulate effective
screening strategies for the early detection of diabetes and
diabetic retinopathy. This would minimize the occurrence of
avoidable blindness in developing nations such as India.
Acknowledgments
We acknowledge the support of the Lions Clubs International
Foundation (LCIF) and RD Tata Trust, Mumbai, for providing grants
to support this project.
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Source of Support: Lions Clubs International Foundation (LCIF)
and RD Tata Trust, Mumbai. Conflict of Interest: None declared.
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JPEG is the most suitable file format. The image quality should be good enough to judge the scientific value of the image. For the purpose
of printing, always retain a good quality, high resolution image. This high resolution image should be sent to the editorial office at the time
of sending a revised article.
4) Legends:
Legends for the figures/images should be included at the end of the article file.
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J Postgrad Med April 2009 Vol 55 Issue 2