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Prevalence of Refractive Errors and Associated

Risk Factors in Subjects with Type 2 Diabetes


Mellitus
SN-DREAMS, Report 18
Padmaja Kumari Rani, MS, FNB (Retina),1 Rajiv Raman, MS, DNB,1 Sudhir R. Rachapalli, MS, MPH,2
Vaitheeswaran Kulothungan, MSc, MPhil,2 Govindasamy Kumaramanickavel, MD,3
Tarun Sharma, MD, FRCSEd, MBA1

Purpose: To report the prevalence of refractive errors and the associated risk factors in subjects with type
2 diabetes mellitus from an urban Indian population.
Design: Population-based, cross-sectional study.
Participants: One thousand eighty participants selected from a pool of 1414 subjects with diabetes.
Methods: A population-based sample of 1414 persons (age ⬎40 years) with diabetes (identified as per the
World Health Organization criteria) underwent a comprehensive eye examination, including objective and
subjective refractions.
Main Outcome Measures: One thousand eighty subjects who were phakic in the right eye with best
corrected visual acuity of ⱖ20/40 were included in the analysis for prevalence of refractive errors. Univariate and
multivariate analyses were done to find out the independent risk factors associated with the refractive errors.
Results: The mean refraction was ⫹0.20⫾1.72, and the Median, ⫹0.25 diopters. The prevalence of em-
metropia (spherical equivalent [SE], ⫺0.50 to ⫹0.50 diopter sphere [DS]) was 39.26%. The prevalence of myopia
(SE ⬍⫺0.50 DS), high myopia (SE ⬍⫺5.00 DS), hyperopia (SE ⬎⫹0.50 DS), and astigmatism (SE ⬍⫺0.50 cyl)
was 19.4%, 1.6%, 39.7%, and 47.4%, respectively. The advancing age was an important risk factor for the three
refractive errors: for myopia, odds ratio (OR; 95% confidence interval [CI] 4.06 [1.74 –9.50]; for hyperopia, OR
[95% CI] 5.85 [2.56 –13.39]; and for astigmatism, OR [95% CI] 2.51 [1.34 – 4.71]). Poor glycemic control was
associated with myopia (OR [95% CI] 4.15 [1.44 –11.92]) and astigmatism (OR [95% CI] 2.01 [1.04 –3.88]). Female
gender was associated with hyperopia alone) OR [95% CI] 2.00 [1.42–2.82].
Conclusions: The present population-based study from urban India noted a high prevalence of refractive
errors (60%) among diabetic subjects ⬎40 years old; the prevalence of astigmatism (47%) was higher than
hyperopia (40%) or myopia (20%).
Financial Disclosure(s): The authors have no proprietary or commercial interest in any of the materials
discussed in this article. Ophthalmology 2010;117:1155–1162 © 2010 by the American Academy of Ophthalmology.

Refractive errors, especially uncorrected ones, are among viduals with older onset diabetes, included cataract, glau-
the most common causes of visual impairment in the world; coma, and macular degeneration.3
the World Health Organization estimates this population to Although there are several reports on prevalence of re-
be around 153 million.1 All refractive errors, however, need fractive errors in the general population, only limited data
not be corrected for a person to have normal function and exist about this in population with diabetes.4 –10 Therefore,
this is especially true if the fellow eye vision is 20/20. the present, population-based study is aimed at estimating
The US Centers for Disease Control and Prevention the prevalence and associated clinical and biochemical risk
reported that among individuals aged ⱖ20 years with factors for refractive errors in populations with type 2
diabetes, 11% had visual impairment (i.e., presenting diabetes.
visual acuity ⬍20/40 in their better-seeing eye while
wearing glasses or contact lenses, if applicable), and
about 65.5% of these cases were correctable.2 In individ- Materials and Methods
uals with younger onset diabetes, diabetic retinopathy Study subjects were recruited from the Sankara Nethralaya Dia-
was responsible for visual acuity of ⬍20/200 in around betic Retinopathy Epidemiology and Molecular Genetic Study.
80% of the eyes, whereas in individuals with older onset The study design and research methodology is described in detail
diabetes, this was the case in one third.3 Important causes elsewhere.11 The study area was the Chennai metropolis with a
of visual impairment, present in nearly half of the indi- population of 4.3 million distributed in 155 divisions of 10 zones.

© 2010 by the American Academy of Ophthalmology ISSN 0161-6420/10/$–see front matter 1155
Published by Elsevier Inc. doi:10.1016/j.ophtha.2009.10.025
Ophthalmology Volume 117, Number 6, June 2010

As a sample, a total of 5999 subjects selected from the general The visual impairment rate owing to refractive errors in the
population aged ⱖ40 years was enumerated; multistage, random study population was ascertained as per the definition of low vision
sampling was stratified on the basis of economic criteria. The and blindness, recommended by the World Health Organization
socioeconomic score was assessed using a multiindex question- (low vision, 6/18 –3/60 and blindness, ⬍3/60; visual impairment
naire. The sample was stratified based on socioeconomic scoring: included both low vision and blindness data).14
low (0 –14), middle (15–28), or high (29 – 42).12 The data were
compared between responders (1563 who visited the base hospital)
and nonresponders (253 who did not visit the base hospital) with Definitions of Biochemical Variables
regard to mean age, gender, diabetes status, and mean fasting Patients were considered to be newly diagnosed diabetics if the
blood sugar levels. No differences were observed. fasting blood glucose level was ⱖ110 mg/dL on 2 occasions.13
Of the 5999 subjects enumerated, 1414 persons identified with Patients were considered to be known diabetics if they were using
diabetes, as per World Health Organization criteria13 (both known hypoglycemic drugs, either oral or insulin, or both.9 Glycemic
and newly diagnosed), were analyzed for the study (96.20% re- control was categorized as normal (glycosylated hemoglobin
sponse rate for first fasting blood sugar estimation, 85.60% re- [HbA1c] ⬍5.6), good (HbA1c 5.6 –7.0), fair (HbA1c 7.1– 8.0),
sponse rate for base hospital examination, 8.7% turned out as unsatisfactory (HbA1c 8.1–10.0), or poor (HbA1c ⬎10).13 High
nondiabetic after second blood sugar and 0.78% of retinal images fasting plasma glucose was considered if the value was ⬎126
were nongradable). The study was approved by the Institutional mg/dL.15 All subjects underwent measurement of height and
Review Board, and an informed consent was obtained from sub- weight, after which the body mass index was calculated using the
jects as per the Declaration of Helsinki. formula: weight (kg)/height (m2). Based on body mass index,
individuals were classified as lean (male, ⬍20; female, ⬍19),
Visual Acuity and Refractive Status Assessment normal (male, 20 –25; female, 19 –24), overweight (male, 25–30;
female, 24 –29) or obese (male, ⬎30; female, ⬎29).16 Educational
Visual acuity was estimated using the modified Early Treatment of status was classified as illiterate, primary education (1–5), higher
Diabetic Retinopathy Study chart (Light House Low Vision Prod- secondary education (6 –12), or college degree or higher.17
ucts, New York, NY); for those who could not read the English
alphabet, Landolt’s ring test was used. Objective refraction (streak
retinoscope, Beta 200, Heine, Germany) was always followed by Statistical Analysis
a subjective one. If the subject was unable to read the 4/40
Statistical analyses were performed using the statistical software
(logarithm of the minimum angle of resolution, 1.0) line, vision
(SPSS for Windows, ver. 13.0 SPSS Science, Chicago, IL). The
was checked at one meter, and if the subject was still unable to
results were expressed as mean values ⫾ SD if the variables were
identify any of the largest optotypes, perception of hand move-
continuous, and as percentage, if categorical. The Student t-test for
ments was checked; and if the vision was less than hand move-
comparing continuous variables, and the chi-square test, for com-
ments, perception of light was tested. Only the right eye of each
paring proportions amongst groups were used. The newly diag-
subject was considered, and of these, phakic eyes with best cor-
nosed diabetics were given a value of zero for the duration of
rected visual acuity ⱖ20/40 (logarithm of the minimum angle of
diabetes. Both univariate and multivariate logistic regression anal-
resolution 0.3) were included for analysis. Thus, a total of 1080
yses were performed to study the effect of various risk factors
subjects were included for estimation of prevalence of refractive
using refractive error and its components—astigmatism, myopia,
error. We considered 20/40 as a cutoff point to prevent the con-
and hyperopia—as dependent variables. From the univariate anal-
founding effect of nuclear sclerosis on refractive error estimation
ysis, variables with P values ⱕ0.05 and those that were already
as well as to compare our study results with other epidemiologic
established as risk factors were included in the multivariate logistic
studies done in the general population.
regression analysis to derive the parsimonious model. Pⱕ0.05 was
In the overall study group (n ⫽ 1414), refraction data were
considered significant.
available for 1379 subjects; 35 subjects were excluded because
refraction was not done (owing to blind eye or media opacity).
Refractive errors were compared between the overall group (n ⫽
1379) and the study group (n ⫽ 1080). Results

Definitions of Clinical Variables Out of the 1414 subjects with diabetes, 1232 (87.1%) were phakic
in the right eye. The remaining 182 (12.9%) subjects had a history
Emmetropia was defined as a spherical equivalent between ⫺0.50 of cataract surgery and were either pseudophakic or aphakic in the
and ⫹0.50 diopter sphere (DS).10 Myopia was defined as a spher- right eye. Of the 1232 phakic subjects, 1080 (76.37%) were
ical equivalent of less than ⫺0.50 DS, and high myopia, a spher- eligible for assessment of refractive status with best corrected
ical equivalent of less than ⫺5.00 DS.4,10 Hyperopia was defined vision of ⱖ20/40. The remaining 152 (12.34%) subjects had visual
as a spherical equivalent of greater than ⫹0.50 DS, and high acuity ⬍20/40: 136 owing to cataract (LOCS III grade ⱖ N2,
hyperopia, a spherical equivalent of more than ⫹5.00 DS.4,10 ⱖC3, ⱖP2), and 16 owing to other ocular diseases.
Astigmatic correction was prescribed in the minus cylinder format, Overall, the mean objective refraction in study subjects
and astigmatism was defined as a cylindrical error less than ⫺0.50 was ⫹0.34⫾1.79, and the mean subjective refraction was
diopter cylinder in any axis.4,10 Astigmatism was defined as with- ⫹0.20⫾1.72. There was no significant difference between the
the-rule if the axis lay between 15° on either side of the horizontal mean objective and subjective refraction (P⫽0.07); refraction data
meridian, against-the-rule if the axis lay between 15° on either side were analyzed based on subjective refraction. The mean refraction
of the vertical meridian, and oblique if the axis lay between 15° between the right and left eye was not significant (Pearson corre-
and 75° or between 105° and 165°.4,10 Grading of lens opacities lation, 0.845). Hence, the right eye alone was considered for
was performed by using the Lens Opacities Classification System assessment of refractive status.
(LOCS) III (LOCS chart III, Leo T. Chylack, Harvard Medical The mean age of the included 1080 subjects was 53.7⫾8.9
School, Boston, MA); significant nuclear sclerosis was defined as years (range, 40 – 81). The mean age of men and women was
nuclear opalescence of ⱖN2. 54.5⫾9.4 and 52.8⫾8.2 years, respectively (P ⫽ 0.001).

1156
Rani et al 䡠 Refractive Errors in Type 2 Diabetes Mellitus

Table 1. Age- and Gender-specific Distribution of Refractive Errors among Persons with Type 2 Diabetes Mellitus

Myopia Hyperopia High Myopia Astigmatism


With- Against-
P P P P Oblique P the-rule P the-rule P
Age Group n n (%) Value n (%) Value n (%) Value Overall Value n (%) Value n (%) Value n (%) Value
Overall
40–49 379 74 (19.5) 78 (20.6) 7 (1.8) 125 (33.0) 20 (24.7) 10 (50.0) 95 (23.1)
50–59 423 68 (16.1) 197 (46.5) 5 (1.2) 222 (52.5) 40 (49.4) 5 (25.0) 177 (43.1)
60–69 216 45 (20.8) 129 (59.7) 4 (1.9) 127 (58.8) 15 (18.5) 5 (25.0) 107 (26.0)
⬎69 62 23 (37.1) 25 (40.3) 1 (1.6) 38 (61.3) 6 (7.4) 0 (0.0) 32 (7.8)
Subtotal 1080 210 (19.4) 0.032 429 (39.7) ⬍0.0001 17 (1.6) 0.915 512 (47.4) ⬍0.0001 81 (15.8) 0.459 20 (3.9) 0.036 411 (80.3) 0.089
Men
40–49 208 45 (21.6) 37 (18.3) 4 (1.9) 72 (34.6) 11 (23.9) 7 (50.0) 54 (23.0)
50–59 216 44 (20.4) 81 (37.5) 3 (1.4) 117 (54.2) 18 (39.1) 2 (14.3) 97 (41.3)
60–69 131 29 (22.1) 70 (53.4) 2 (1.5) 80 (61.1) 11 (23.9) 5 (35.7) 64 (27.4)
⬎69 43 18 (41.9) 14 (32.6) 1 (2.3) 26 (60.5) 6 (13.0) 0 (0.0) 20 (8.5)
Subtotal 598 136 (22.7) 0.058 203 (34.0) ⬍0.0001 10 (1.7) 0.959 295 (49.3) ⬍0.0001 46 (15.6) 0.641 14 (4.7) 0.144 235 (79.7) 0.726
Women
40–49 171 29 (17.0) 40 (23.4) 3 (1.8) 53 (31.0) 9 (25.7) 3 (50.0) 41 (23.3)
50–59 207 24 (11.6) 115 (56.1) 2 (1.0) 105 (50.7) 22 (62.9) 3 (50.0) 80 (45.5)
60–69 85 16 (18.8) 59 (69.4) 2 (1.0) 47 (55.3) 4 (11.4) 0 (0.0) 43 (24.4)
⬎69 19 5 (26.3) 11 (57.9) 0 (0.0) 12 (63.2) 0 (0.0) 0 (0.0) 12 (6.8)
Subtotal 482 74 (15.4) 0.503 226 (46.9) ⬍0.0001 7 (1.5) 0.889 217 (45.0) ⬍0.0001 35 (16.1) 0.076 6 (2.8) 0.078 176 (81.1) 0.016

Myopia was defined as a spherical equivalent of less than ⫺0.50 diopter sphere (DS). Hyperopia was defined as a spherical equivalent of greater than ⫹0.50
DS. High myopia was defined as less than ⫺5.00 D. Astigmatism was defined as a cylindrical error less than ⫺0.50 diopter cylinder (DC) in any axis.
Astigmatism was defined as with-the-rule if the axis lay between 15° on either side of the horizontal meridian, against-the rule if the axis lay between 15°
on either side of the vertical meridian, and oblique if the axis lay between 15° and 75° or between 105° and 165°.

The prevalence of emmetropia was 39.3% (424/1080; 95% CI, (411/512). The prevalence of astigmatism increased significantly
36.4 – 42.2); the prevalence, after adjusting for age and gender for with age (chi-square for trend, P⬍0.0001) in the overall group. In
the urban Chennai population was 39.9% (95% CI, 39.9 – 40.1). subjects having oblique astigmatism, age and gender did not in-
The prevalence of emmetropia decreased significantly with in- fluence the prevalence; in subjects having with-the-rule astigma-
creasing age (chi-square test for trend P⬍0.0001). There were 249 tism, the prevalence decreased with age in the overall group
men (41.6% of all men) and 175 women (36.3% of all women) in (P⫽0.04) and no difference was noted regarding gender; in sub-
the emmetropia group. jects having against-the-rule, the prevalence decreased with age,
Table 1 shows age- and gender-specific distribution of refractive only in women (P⫽0.02), and no difference was noted in the
errors in subjects with type 2 diabetes. The overall prevalence of myopia overall group and in men.
was 19.4% (95% CI, 17.1–21.8), and that of high myopia, 1.6% (95% CI, Table 2 shows the univariate analysis of the risk factors for
0.8–2.3). The prevalence of myopia and high myopia, after adjusting for refractive errors in persons with type 2 diabetes. Clinical param-
age and gender for the urban Chennai population, was 20.4% (95% CI, eters that were significantly associated with myopia included in-
20.4–20.5) and 1.6% (95% CI, 1.6–1.6), respectively. The mean age of creasing age, primary education, and nuclear sclerosis (⬎2); sig-
subjects with myopia was 55.1⫾10.2 years, and that of the entire popu- nificant biochemical parameter was poor glycemic control. For
lation, 53.8⫾8.5 years (P⫽0.015). The mean age of subjects with high hyperopia, significant clinical variables were increasing age, fe-
myopia was 53.8⫾ 8.9 years, and that of the entire population, 53.8⫾8.5 male gender, known diabetes, increased duration of diabetes, nu-
years (P⫽0.666). The prevalence of myopia increased significantly with clear sclerosis (⬎2); a significant biochemical variable was low
age (chi-square for trend, P⫽0.032). With regard to gender, there was no fasting plasma glucose levels. For astigmatism (all types) and in a
difference in the prevalence of myopia and high myopia. subgroup of individuals with against-the-rule astigmatism, signif-
The overall prevalence of hyperopia was 39.7% (95% CI, icant clinical variables were advanced age, greater duration of
36.4 – 42.6), and that of high hyperopia, 0.2% (95% CI, ⫺0.1 to diabetes, significant nuclear sclerosis, and diabetic retinopathy; a
0.5). The prevalence of hyperopia, after the age and gender were significant biochemical variable was poor glycemic control.
adjusted for the urban Chennai population, was 37.9% (95% CI, Table 3 shows significant risk factors found on multiple logistic
37.9 –38.1). Hyperopia was more prevalent among women (46.9 vs regression analyses. Increased age was significantly associated
34.0; P⬍0.0001). The mean age of subjects with hyperopia was with all types of refractive errors: myopia, hyperopia, and astig-
56.5⫾7.9 years, and that of the entire population, 51.9⫾9.1 years matism (all types) and against-the-rule astigmatism. For myopia,
(P⬍0.0001). The prevalence of hyperopia increased significantly presence of diabetes for ⬎15 years showed an inverse relation OR
with age (chi-square for trend P⬍0.0001) through the age of 69 (0.38; 95% CI, 0.18 – 0.81); increasing prevalence of myopia was
years; thereafter, it showed little decline. noted as the glycemic control worsened from good to poor. For
The prevalence of astigmatism was 47.4% (95% CI, 44.4 – hyperopia, female gender showed an increased prevalence (OR,
50.4). The prevalence of astigmatism, after the age and gender 2.00; 95% CI, 1.42–2.82).
adjustment for the Chennai population, was 46.2% (95% CI, Astigmatism (all types) showed an increased prevalence with
46.2– 46.3). Astigmatism was more prevalent among men (49.3 vs poor glycemic control (OR, 2.01; 95% CI, 1.04 –3.88). In subjects
45.0; P⬍0.0001). Oblique astigmatism was seen in 15.8% (81/ with against-the-rule astigmatism, increased duration of diabetes
512); with-the-rule in 3.9% (20/512) and against-the-rule in 80.3% ⬎15 years was a risk factor (OR, 1.67; 95% CI, 1.05–2.67).

1157
Ophthalmology Volume 117, Number 6, June 2010

Table 2. Univariate Analysis of Risk Factors for Refractive Errors in Persons with Type 2 Diabetes

Against-the-rule
Myopia Hyperopia Astigmatism Astigmatism
Variables n OR (95% CI) n OR (95% CI) n OR (95% CI) n OR (95% CI)
Clinical variables
Age groups (yrs)
40–49 81 1.00 78 1.00 125 1.00 95 1.00
50–59 73 1.29 (0.89–1.89) 197 3.63 (2.60–5.07)* 222 2.24 (1.68–2.99)* 177 2.15 (1.59–2.91)*
60–69 49 3.50 (2.14–5.74)* 129 9.58 (6.14–14.93)* 127 2.90 (2.05–4.09)* 107 2.93 (2.06–4.18)*
ⱖ70 24 5.01 (2.43–10.32)* 25 5.42 (2.64–11.12)* 38 3.22 (1.85–5.59)* 32 3.19 (1.84–5.52)*
Gender
Male 146 1.00 203 1.00 295 1.00 235 1.00
Female 81 0.79 (0.57–1.10) 226 1.58 (1.21–2.08)* 217 0.84 (0.66–1.07) 176 0.89 (0.69–1.14)
Educational status
Illiterate 3 1.00 21 1.00 16 1.00 15 1.00
Primary (1 to 5) 48 4.00 (1.09–14.62)* 64 0.76 (0.36–1.61) 89 1.54 (0.76–3.12) 75 1.24 (0.61–2.52)
Higher Secondary (6–12) 124 2.40 (0.68–8.45) 261 0.72 (0.36–1.43) 307 1.31 (0.68–2.53) 241 0.96 (0.49–1.86)
Degree and more 52 2.86 (0.79–10.33) 83 0.65 (0.31–1.35) 100 1.14 (0.57–2.27) 80 0.88 (0.43–1.77)
BMI (kg/m2)
Normal 92 1.00 149 1.00 191 1.00 157 1.00
Lean 13 1.14 (0.54–2.43) 25 1.36 (0.72–2.57) 30 1.19 (0.68–2.07) 24 1.10 (0.63–1.94)
Overweight 92 0.86 (0.60–1.24) 189 1.09 (0.81–1.49) 220 0.98 (0.75–1.29) 176 0.94 (0.72–1.24)
Obese 30 0.69 (0.42–1.13) 66 0.93 (0.62–1.39) 71 0.77 (0.54–1.11) 54 0.71 (0.49–1.04)
Diabetes status
Newly detected 57 1.00 62 1.00 90 1.00 341 1.00
Known diabetes 170 0.88 (0.61–1.29) 367 1.76 (1.23–2.49)* 422 1.34 (0.99–1.81) 70 1.36 (0.99–1.86)
Duration of diabetes (yrs)
⬍5 150 1.00 238 1.00 284 1.00 221 1.00
5–10 40 0.93 (0.60–1.43) 76 1.11 (0.78–1.59) 107 1.62 (1.18–2.24)* 87 1.61 (1.16–2.23)*
10–15 23 1.32 (0.74–2.33) 62 2.24 (1.41–3.55)* 54 1.14 (0.77–1.69) 46 1.29 (0.86–1.94)
ⱖ15 14 0.67 (0.35–1.29) 53 1.61 (1.03–2.53)* 67 2.35 (1.54–3.60)* 57 2.37 (1.57–3.60)*
Lens status
Significant nuclear sclerosis (ⱕ2) 99 1.00 188 1.00 221 1.00 175 1.00
Significant nuclear sclerosis (⬎2) 128 2.13 (1.53–2.96)* 241 2.11 (1.61–2.78)* 291 1.83 (1.43–2.32)* 236 1.73 (1.35–2.22)*
Diabetic retinopathy
No diabetic retinopathy 187 1.00 349 1.00 409 1.00 326 1.00
Diabetic retinopathy 40 1.18 (0.77–1.82) 80 1.27 (0.88–1.81) 103 1.49 (1.08–2.05)* 85 1.48 (1.08–2.04)*
Biochemical variables
HbA1c (g%)
⬍5.6 6 1.00 31 1.00 23 1.00 19 1.00
5.6–7.0 63 2.87 (1.14–7.24)* 140 1.23 (0.71–2.14) 144 1.64 (0.95–2.83) 116 1.49 (0.84–2.66)
7.1–8.0 41 2.88 (1.11–7.45)* 79 1.07 (0.59–1.93) 96 1.92 (1.08–3.41)* 77 1.70 (0.93–3.11)
8.1–10.0 69 2.85 (1.14–7.16)* 106 0.85 (0.47–1.48) 145 1.82 (1.05–3.16)* 117 1.65 (0.92–2.93)
⬎10.0 48 3.66 (1.42–9.42)* 73 1.08 (0.59–1.95) 104 2.39 (1.34–4.25)* 82 1.98 (1.08–3.61)*
Fasting plasma glucose (mg/dL)
⬍126 91 1.00 212 1.00 214 1.00 174 1.00
ⱖ126 136 0.98 (0.71–1.36) 217 0.67 (0.51–0.88)* 298 1.15 (0.90–1.46) 237 1.09 (0.85–1.39)

BMI ⫽ body mass index; CI ⫽ confidence interval; FPG ⫽ fasting plasma glucose; HbA1c ⫽ glycosylated hemoglobin; OR ⫽ odds ratio.
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).
*P⬍0.05.

Table 4 shows comparative analysis of refractive errors be- Discussion


tween the overall group (n ⫽ 1379) and the study population (n ⫽
1080). The prevalence of myopia was higher in the overall group
(24.1% vs 19.4%; P⫽0.005) and in women (21.9% vs 15.4%; The present, population-based study found that the preva-
P⫽0.006); no differences were observed with other refractive errors. lence of all types of refractive errors in type 2 diabetes
Table 5 shows visual impairment rate due to refractive errors in mellitus was about 60%. The prevalence of myopia, hyper-
the overall population. Visual impairment rate (defined as visual opia, and astigmatism in the study population with type 2
acuity of ⬍6/18) was 6.2% in the right eye and 3.3% in both eyes.
In the right eye, contributing refractive errors to visual impairment
diabetes mellitus was 20%, 40%, and 47%, respectively. We
included astigmatism (33.7%), myopia (31.4%), hyperopia attempted to extrapolate these prevalence estimates to the
(26.7%), and high myopia (8.1%); and in both eyes, contributing urban population of India. Based on the 2001 census, the
refractive errors were myopia (35.6%), astigmatism (31.1%), hy- urban population was 286 million. Of these, about 114
peropia (24.4%), and high myopia (8.9%). million were over age 30.18 Assuming the current preva-

1158
Rani et al 䡠 Refractive Errors in Type 2 Diabetes Mellitus

Table 3. Multivariate Analysis of Risk Factors for Refractive Errors in Persons with Type 2 Diabetes

Against-the-rule
Myopia Hyperopia Astigmatism Astigmatism
Variables OR (95% CI) OR (95% CI) OR (95% CI) OR (95% CI)
Clinical variables
Age group (yrs)
40–49 1.00 1.00 1.00 1.00
50–59 1.24 (0.81–1.89) 3.61 (2.51–5.19)* 2.03 (1.49–2.77)* 1.95 (1.41–2.69)*
60–69 3.16 (1.71–5.86)* 10.67 (6.31–18.07)* 2.36 (1.56–3.56)* 2.41 (1.58–3.66)*
ⱖ70 4.06 (1.74–9.50)* 5.85 (2.56–13.39)* 2.51 (1.34–4.71)* 2.46 (1.31–4.59)*
Gender
Male 1.00 1.00 1.00 1.00
Female 0.85 (0.57–1.28) 2.00 (1.42–2.82)* 0.84 (0.63–1.11) 0.91 (0.68–1.21)
Educational status
Illiterate 1.00 1.00 1.00 1.00
Primary (1–5) 3.46 (0.89–13.45) 0.71 (0.31–1.62) 1.65 (0.79–3.45) 1.34 (0.64–2.81)
Higher secondary (6–12) 2.37 (0.63–8.92) 0.91 (0.43–1.93) 1.41 (0.70–2.81) 1.03 (0.52–2.07)
Degree and more 3.17 (0.82–12.32) 0.89 (0.39–2.02) 1.24 (0.59–2.59) 0.96 (0.46–2.01)
BMI (kg/m2)
Normal 1.00 1.00 1.00 1.00
Lean 1.10 (0.48–2.50) 1.17 (0.58–2.34) 1.08 (0.60–1.95) 1.01 (0.56–1.82)
Overweight 0.94 (0.63–1.39) 1.02 (0.72–1.45) 1.14 (0.85–1.53) 1.07 (0.79–1.44)
Obese 0.90 (0.51–1.60) 0.85 (0.52–1.38) 1.03 (0.68–1.55) 0.89 (0.58–1.37)
Diabetes status
Newly detected 1.00 1.00 1.00 1.00
Known diabetes 0.91 (0.58–1.43) 1.46 (0.94–2.25) 1.07 (0.75–1.51) 1.03 (0.72–1.49)
Duration of diabetes (yrs)
⬍5 1.00 1.00 1.00 1.00
5–10 0.83 (0.51–1.35) 0.67 (0.44–1.04) 1.38 (0.97–1.97) 1.39 (0.97–1.98)
10–15 0.94 (0.48–1.83) 1.52 (0.88–2.63) 0.88 (0.57–1.37) 1.03 (0.66–1.61)
ⱖ15 0.38 (0.18–0.81)* 0.67 (0.38–1.18) 1.61 (0.99–2.59) 1.67 (1.05–2.67)*
Lens status
Significant nuclear 1.00 1.00 1.00 1.00
sclerosis (ⱕ2)
Significant nuclear 1.29 (0.85–1.98) 1.02 (0.72–1.44) 1.19 (0.89–1.59) 1.11 (0.82–1.49)
sclerosis (⬎2)
Diabetic retinopathy
No diabetic retinopathy 1.00 1.00 1.00 1.00
Diabetic retinopathy 1.25 (0.75–2.08) 1.19 (0.77–1.84) 1.17 (0.81–1.67) 1.19 (0.83–1.70)
Biochemical variables
HbA1c (g%)
⬍5.6 1.00 1.00 1.00 1.00
5.6–7.0 2.94 (1.11–7.80)* 1.39 (0.75–2.60) 1.70 (0.96–3.01) 1.57 (0.86–2.86)
7.1–8.0 2.89 (1.04–8.04)* 1.14 (0.57–2.28) 1.71 (0.92–3.18) 1.55 (0.81–2.96)
8.1–10.0 2.99 (1.08–8.31)* 1.05 (0.52–2.11) 1.66 (0.89–3.10) 1.52 (0.79–2.91)
⬎10.0 4.15 (1.44–11.92)* 1.21 (0.57–2.54) 2.01 (1.04–3.88)* 1.66 (0.84–2.29)
Fasting plasma glucose
(mg/dL)
⬍126 1.00 1.00 1.00 1.00
ⱖ126) 0.92 (0.59–1.41) 0.83 (0.56–1.22) 1.12 (0.82–1.54) 1.08 (0.78–1.49)

BMI ⫽ body mass index; CI ⫽ confidence interval; FPG ⫽ fasting plasma glucose; HbA1c ⫽ glycosylated
hemoglobin; OR ⫽ odds ratio.
*P ⬍ 0.05.

lence of diabetes mellitus to be around 28% (in urban Transient refractive error shift, in association with
Chennai, above the age of 40 years),19 there would be plasma glucose concentration, has been reported in clinical
approximately a 32 million-person cohort of diabetic indi- studies; usually myopia occurs with hyperglycemia, and
viduals in urban India. Of these 32 million subjects with hyperopia, with hypoglycemia.20,21 However, how common
diabetes, around 6.4 million will have myopia, about 12.8 the occurrence of refractive errors in population with dia-
million will have hyperopia, and approximately 15 million betes is not well-reported. A community-based study from
will have astigmatism. However, we note that the present Taiwan (n ⫽ 547; ⬎40 years of age) in self-reported sub-
study had a limitation of not collecting the data on the use jects with diabetes reported prevalence of myopia (44.1%),
of spectacles and habitual visual acuity. hyperopia (24.1%), and astigmatism (87.8%).3 However,

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Ophthalmology Volume 117, Number 6, June 2010

Table 4. Comparison of Prevalence of Refractive Errors


between the Overall Group* and the Study Group†

Overall Group Study Group


Variables (1379) % (1080) % P Value
Myopia 24.1 19.4 0.005
High myopia 2.3 1.6 0.189
Hypermetropia 36.2 39.7 0.073
Astigmatism 50.4 47.4 0.141
Men
Myopia 26.1 22.7 0.154
High myopia 3 1.7 0.117
Hypermetropia 31.7 34 0.385
Astigmatism 51.2 49.3 0.507
Women Figure 1. Refractive error status comparison among persons with type 2
Myopia 21.9 15.4 0.006
diabetes (present study vs Taiwan study). Same definition of Taiwan study
High myopia 1.6 1.5 0.891
applied to our study data. Refractive error was defined as myopia ⱕ0.50
Hypermetropia 41.3 46.9 0.062
diopters (D) and as hyperopia ⱖ0.50 D. Emmetropia between ⫺0.50 D and
Astigmatism 49.5 45 0.133
⫹0.50D and high myopia was defined as less than ⫺6.00 D. Astigmatism was
defined as a cylindrical error ⱕ0.50 diopter cylinder (DC) in any axis.
*Overall group (n ⫽ 1379) includes refractive error data from the right eye
with inclusion of all visual acuities (including ⱕ20/40) and any lens status
(phakics, aphakics, and pseudopahkics) in the total study population.

Study group (n ⫽ 1080) includes refractive error data from the right eye, the Taiwan study; however, hyperopia was more common in
phakic status and visual acuity ⱖ20/40. our study (45.6% vs 24.1%). Ethnic differences could also be
a possible reason for the higher prevalence of high myopia in
the Taiwan study.3,22,23
there were several differences between their study and the Table 6 compares the data of the present study (popula-
present one. Their population was from self-reported indi- tion with diabetes) with the prevalence data of refractive
viduals, whereas ours is a true epidemiologic study with errors in various reported series (general population). The
⬎1000 subjects being analyzed. Second, the definition of prevalence of emmetropia in the present study was noted
refractive errors was different; in our study, myopia and hy- to be around 40% compared with around 25% to 30%
peropia have been defined as a spherical equivalent of less than reported from Chennai Glaucoma Study, Beaver Dam
⫺0.50 DS and more than ⫹0.50 DS, respectively, whereas in Study, Blue Mountain Study, and Tanjog Pagar Singa-
their study, the definition included myopia ⫺0.50 DS or lower pore study.5,22,24,25 This finding suggests that diabetes
and hyperopia ⫹0.50 DS or greater. Thus, there is the possi- mellitus per se does not make an individual ametropic.
bility of overestimating the prevalence of refractive errors. The prevalence of myopia in the present study (around
When we applied the same definition of refractive errors as 20%) was similar to other studies (around 14%–26%), but
was used in the Taiwan study (Fig 1), we found that the for Singapore study (39%); this high prevalence of myopia
prevalence of astigmatism (87.8% vs 63.4%), myopia (44.1% in Singapore could be due to ethnic differences between the
vs 23.9%), and high myopia (13% vs 1.01%) were higher in 2 populations. The converse was true for hyperopia in

Table 5. Visual Impairment Rates* Owing to Refractive Errors in the Overall Study Population with
Diabetes (n-1379)

Overall Group Myopia High Myopia Hyperopia Astigmatism


(n ⴝ 1379) (n ⴝ 333) (n ⴝ 32) (n ⴝ 499) (n ⴝ 553)
Right eye
Low vision 80 ( 5.8%) 27 6 19 28
Blindness 6 (0.4%) 0 1 4 1
Visual impairment 86 (6.2%) 27 (31.3%) 7 (8.1%) 23 (26.7%) 29 (33.7%)
Both eyes (any 1 better eye)
Low vision 44 (3.2%) 16 3 11 14
Blindness 1(0.07%) 0 1 0 0
Visual impairment 45 (3.3%) 16 (35.5%) 4 (8.9%) 11 (24.4%) 14 (31.1%)

Myopia was defined as a spherical equivalent of less than ⫺0.50 diopter sphere (DS). Hyperopia was defined as a spherical
equivalent of greater than ⫹0.50 DS. High myopia was defined as less than ⫺5.00 D. Astigmatism was defined as a
cylindrical error less than ⫺0.50 diopter cylinder (DC) in any axis. Astigmatism was defined as with-the-rule if the axis
lay between 15° on either side of the horizontal meridian, against- the rule if the axis lay between 15° on either side of the
vertical meridian, and oblique if the axis lay between 15° and 75° or between 105° and 165°.
*Visual impairment rate owing to refractive errors in the study population was ascertained as per the definition of low
vision and blindness, recommended by the World Health Organization (Low vision, 6/18 –3/60; blindness, ⬍3/60;
and visual impairment included both low vision and blindness data).

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Rani et al 䡠 Refractive Errors in Type 2 Diabetes Mellitus

Table 6. Comparison of Prevalence Data of Refractive Errors between the Present Study (Population
with Diabetes) and Various Published Studies (General Population)

Age Emmetropia Myopia Hyperopia Astigmatism


Study n (yrs) Population (%) (%) (%) (%)
Present study* 1080 ⱖ40 Type 2 Diabetes 39.2 21.1 39.7 47.4
Chennai Glaucoma 3143 ⱖ40 Urban General 29.4 18.4 52.3 53.0
Study20* population
Beaver Dam study5* 4275 ⱖ40 General population 24.8 26.2 49.0 NR
Blue mountain 3174 ⱖ50 General population 28.6 14.4 57.0 NR
study25*
Tanjog Pagar 1232 ⱖ40 General population 32.9 38.7 28.4 37.8
Singapore22*

NR ⫽ Not reported.
*Myopia was defined as a spherical equivalent of less than ⫺0.50 diopter sphere (DS). Hyperopia was defined as a
spherical equivalent of greater than ⫹0.50 DS. Astigmatism was defined as a cylindrical error less than ⫺0.50 diopter
cylinder (DC) in any axis. Astigmatism was defined as with-the-rule if the axis lay between 15° on either side of the
horizontal meridian, against- the rule if the axis lay between 15° on either side of the vertical meridian, and oblique
if the axis lay between 15° and 75° or between 105° and 165°.

Singapore (around 28%); the prevalence of hyperopia in the known diabetes status were associated with hyperopia on
present study was somewhat less compared with other series univariate analysis. The influence of low plasma glucose
(around 40% vs 52%, 49%, 57%). The prevalence of astig- (both acute and chronic) inducing hyperopic shift is a
matism was higher in the general population of Chennai known phenomenon.20 We found an inverse relationship
compared with the present study (53% vs 47%); however, between myopia prevalence and increased duration of dia-
the prevalence was lower in Singapore (around 38%). The betes (⬎15 years). A similar finding was observed in a study
exact reason for these differences in the prevalence esti- conducted in persons with type 1 diabetes.27
mates is unknown. It could be because of the influence of Astigmatism, especially against-the-rule (nearly 80%),
biochemical variables such as blood glucose and glycosy- was found in the present study, and this could be due to the
lated hemoglobin on the refractive status in population with reduced lid laxity (age-related) resulting in flattening of
diabetes;20,21 however, to prove such a cause and effect vertical meridian of the cornea.28,29 Risk of astigmatism
relationship, longitudinal studies are warranted. increased nearly 2-fold in individuals present with poor
Logistic regression analysis revealed advancing age as glycemic control. Apart from age influence, astigmatism in
the most significant risk factor common to all the refractive diabetes may be because of alterations in corneal topogra-
errors—myopia, hyperopia, astigmatism (all types), and phy from blood sugar.21 The presence of diabetic retinopa-
against-the-rule astigmatism. Similar findings were ob- thy and increased duration of diabetes were associated with
served in studies conducted worldwide in the general pop- astigmatism only on univariate analysis; significance disap-
ulation as well as in the Taiwan study involving population peared on multivariate analysis.
with diabetes.3-8 Age, as a risk factor, could be due to the One of the important causes of visual impairment in the
biometric changes in the optical system of lens. To prevent general population worldwide is uncorrected refractive er-
a confounding effect of nuclear sclerosis on the prevalence rors. The present study observed that around 6% have visual
of refractive errors, we excluded subjects with visual acuity impairment in 1 eye, and around 3% in both the eyes owing
ⱕ20/40. That is why, even though significant nuclear scle- to refractive errors, in subjects with diabetes, above the age
rosis was found as a common risk factor for the 3 refractive of 40 years. Extrapolating these estimates to approximately
errors on univariate analysis, the significance disappeared 32 million urban subjects with diabetes mellitus, around 2
on multiple logistic regression analysis. million will have visual impairment in 1 eye, and around 1
Worsening of glycemic control resulted in the risk of million in both the eyes. Therefore, creating awareness and
myopia increasing by nearly 4-fold; hyperglycemia causing conducting screening programs for the detection of correct-
myopic shift is a known phenomenon reported earlier.21 able refractive errors and treating them with suitable glasses
Hyperopia showed an increased prevalence through age will have tremendous impact in reducing the magnitude of
69 (10-fold); thereafter, there was a decline (5-fold). A visual impairment in subjects with diabetes mellitus.
similar pattern was found in various studies conducted in
the general population.9,10 This could be because of the References
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Footnotes and Financial Disclosures


Originally received: March 24, 2009. Financial Disclosure(s):
Final revision: October 11, 2009. The authors have no proprietary or commercial interest in any of the
Accepted: October 13, 2009. materials discussed in this article.
Available online: February 16, 2010. Manuscript no. 2009-417.
1
Funded by the RD Tata Trust, Mumbai.
Shri Bhagwan Mahavir Vitreoretinal Services, Sankara Nethralaya,
Chennai, Tamil Nadu, India. Correspondence:
2
Department of Preventive Ophthalmology, Sankara Nethralaya, Chennai, Dr. Tarun Sharma, MD, FRCSEd, MBA, Principal Investigator & Director,
Tamil Nadu, India. Shri Bhagwan Mahavir Vitreoretinal Services, Sankara Nethralaya, 18
3
Department of Molecular Genetics, Sankara Nethralaya, Chennai, Tamil College Road, Chennai, 600006, Tamil Nadu, India. E-mail: drtaruns@
Nadu, India. gmail.com.

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