Indian Journal of Clinical and Experimental Ophthalmology

Print ISSN: 2395-1443

Online ISSN: 2395-1451

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Indian Journal of Clinical and Experimental Ophthalmology (IJCEO) is open access, a peer-reviewed medical journal, published quarterly, online, and in print, by the  Innovative Education and Scientific Research Foundation (IESRF) since 2015. To fulfill our aim of rapid dissemination of knowledge, we publish articles ‘Ahead of Print’ on acceptance. In addition, the journal allows free more...


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Cardoza, Radhakrishnan, Desai, Mohankumar, and Mohan: Association of serum lipid levels and social factors with diabetic retinopathy in patients with type 2 diabetes mellitus: Study from tertiary care center of Western Maharashtra


Introduction

Diabetes mellitus (DM) is a widespread multifactorial disease that imposes a serious burden to our healthcare system. India alone is estimated to have about 69.2 million diabetics and these numbers are predicted to soar as high as 123.5 million by the year 2040.1, 2

Type 2 diabetics include those individuals who are seen to have insulin resistance (IR) and usually relative deficiency of insulin. Diabetes mellitus leads to microvascular and macrovascular complications. Macrovascular abnormalities include coronary vascular disease, stroke and peripheral vascular disease. The microvascular complications include diabetic retinopathy, diabetic nephropathy and diabetic neuropathy. Chronically elevated blood sugar levels, increase in the reactive oxygen species, decrease in the nitric oxides and increase in fatty acids contribute to the chronic vascular complications by changing the vascular response.3

A multitude of risk factors have been studied to understand how DR develops and progresses. These include the type of diabetes mellitus and the duration of the disease, gender, age, body-mass index (BMI), glycemic control, hypertension, nephropathy, smoking, pregnancy and serum lipid levels.4, 5 The importance of serum lipid levels in the development and progression of DR has been assessed worldwide with a lot of variable results. Dyslipidemia, characterized by raised levels of serum total cholesterol (TC), triglycerides (TG), low density lipoprotein cholesterol (LDL-C) and reduced levels of high density lipoprotein cholesterol (HDL-C) have been hypothesized as probable risk factors for DR. Hyperlipidemia is known to cause dysfunction in the endothelium due to reduced nitric oxide and also the breakdown of BRB which leads to lipid exudation and lipoprotein exudation that leads to various changes in DR and leads to diabetic macular edema (DME) formation.6 Diabetic macular edema is a common cause of severe vision loss in diabetic patients.7, 8

Various social factors like occupation, whether the individual lives in a rural or urban locality and education may be associated with diabetic retinopathy. This could be due to changes in lifestyle and diet in these individuals and also due to differences in awareness about the disease and the need for screening. There are also discrepancies in availability of resources and affordability among various social groups.

There have been variations in results and observations from various international studies and there is a scarcity of data from available local literature. Hence, we conducted this study in our tertiary care hospital to explore this interesting relationship between serum lipid levels and other social factors and DR in our local population.

Materials and Methods

A hospital based observational, cross sectional study was conducted in a tertiary hospital and research centre in Western Maharashtra, from September 2018 to August 2020. 200 patients with type 2 diabetes mellitus, aged 30-70 years were included in the study. Participants were segregated into 2 categories:- (i) category-I of patients with diabetic retinopathy and (ii) category-II of patients without diabetic retinopathy.

Patients with type 1 or indeterminate diabetes mellitus, where OCT was not possible due to hazy media or refusals, any prior ocular treatment, concomitant fundus pathology potentially affecting the macula (e.g arterial/venous occlusions),patients having corneal diseases, inflammatory eye diseases, optic neuropathy and age related macular degeneration, any other ocular pathology that could influence the progression of retinopathy (high myopia, glaucoma, retinitis pigmentosa, other causes of optic atrophy, etc.), any history of radiation to the head or neck region, carotid vascular disease detected by carotid doppler and patients on hemo or /peritoneal dialysis were excluded from the study.

Participant information sheet (PIS) regarding details of study were prepared in English and Marathi language. PIS was given to the participants and they were explained in detail about the study in a language best understood by the patient. Participants were enrolled after getting written informed consent.

A Detailed history from each patient was obtained Following data was collected:

  1. Age

  2. Sex

  3. Locality (urban/rural)

  4. Occupation

  5. Education status

Vision was assessed using illuminated Snellen's Chart. Anterior segment was evaluated in detail by slit lamp examination and fundus examination was done in a dark room with indirect ophthalmoscope. Fundus was also evaluated by means of direct ophthalmoscopy and slit lamp biomicroscopy with +90D lens. Fundus camera was used to obtain a fundus photograph. Participants were segregated into 2 categories. Group-1 included patients with type 2 diabetes mellitus with diabetic retinopathy. Group-2 included patients with type 2 diabetes mellitus without diabetic retinopathy. For grading the severity of diabetic retinopathy, Early Treatment Diabetic Retinopathy Study (ETDRS) protocol was followed. For a detailed analysis, the DR group was further divided into patients with NPDR and those with PDR based on the ETDRS protocol.

To measure serum lipid levels, patient was kept fasting for 12 hours (No food or drink, except water). 2 ml of blood was collected from a resting patient using an optimal venopuncture technique in a red vacutainer and serum lipid levels namely serum total cholesterol, HDL cholesterol, LDL cholesterol and triglycerides were measured. Normal range of serum TC is <200mg/dl, serum HDL-C is 35-80mg/dl in males and 42-88mg/dl in females, serum LDL-C is <130mg/dl, serum TG is 40-160 mg/dl. Fasting plasma glucose was measured after an overnight fast(8 hours fasting with no food, drink except water). 2 ml of blood was then collected in a grey vacutainer tube containing sodium fluoride as a preservative and fasting blood glucose was measured. Normal levels of fasting blood glucose range between 70-100 mg/dl. Fasting blood glucose level of 126 mg/dl or above is indicative of diabetes mellitus. To measure HbA1C, 2 ml of blood was collected in a lavender vacutainer containing EDTA as a preservative. Normal level of HbA1C is 4.8-5.9%. HbA1C of 6.5% or higher is indicative of diabetes mellitus. The above lab tests were conducted and results were documented.

All details of participants were kept under strict confidentiality. Data was collected, compiled and tabulated in excel sheet. The categorical variables were presented in number and percentage (%) form and the continuous variables were presented as mean ± SD and median. Normality of the data was tested by Kolmogorov-Smirnov test. If the normality was rejected, then the non-parametric test was used.

Statistical tests were applied as follows:

  1. Quantitative variables were compared using Independent t test/Mann-Whitney Test (when the data sets were not normally distributed) between the two groups.

  2. Qualitative variables were compared using Chi-Square test/Fisher’s Exact test.

A p Value of <0.05 was considered to be statistically significant.

The data was analysed using Statistical Package for Social Sciences (SPSS) version 21.0.

Results

Prevalence of dyslipidemia in our study was 75.50 %( 151 patients).

Mean ± SD of LDL(mg/dL) in diabetic retinopathy was 118.86 ± 40.58mg/dl and 103.97 ± 36.34mg/dl in patients without diabetic retinopathy .Thus significant association was seen between serum LDL levels and diabetic retinopathy.(p=0.006)

Mean ± SD of HDL (mg/dL) in patients with diabetic retinopathy was 38.02 ± 6.43mg/dl and in patients without diabetic retinopathy was 38.34 ± 8.5mg/dl with no significant association between them. (p=0.764)

Mean ± SD of total cholesterol (mg/dL) in diabetic retinopathy was 177.76 ± 56.45mg/dl and in patients without diabetic retinopathy was 168.48 ± 37.55mg/dl and no significant association was seen between them. (p=0.172)

Median (IQR) of Triglyceride (mg/dL) in patients with diabetic retinopathy was 135.5 (118-208.5) mg/dl and in patients without diabetic retinopathy was 144.5 (124.5-186)mg/dl with no significant association between them. (p=0.597)

Patients living in urban areas had more prevalence of diabetic retinopathy in our study. (p<0.0001)

Diabetic retinopathy was more prevalent among clerks and homemakers. (p=0.004)

Patients with primary school and high school education had significant association with diabetic retinopathy. (p=0.007)

Table 1

Prevalence of dyslipidemia of study subjects

Dyslipidemia

Frequency

Percentage

No

49

24.50%

Yes

151

75.50%

Total

200

100.00%

Table 2

Association of lipid profile with diabetic retinopathy

Lipid profile

Diabetic retinopathy(n=100)

No diabetic retinopathy(n=100)

Total

P value

Test performed

Total cholesterol (mg/dL)

Normal

69 (69%)

79 (79%)

148 (74%)

0.107

Chi square test,2.599

Deranged

31 (31%)

21 (21%)

52 (26%)

Mean ± SD

177.76 ± 56.45

168.48 ± 37.55

173.12 ± 48.05

0.172

t test;1.369

Median(IQR)

169(132-210)

166 (134.25-190)

167 (132-201)

Range

108-372

91-269

91-372

HDL(mg/dL)

Normal

46 (46%)

52 (52%)

98 (49%)

0.396

Chi square test,0.72

Deranged

54 (54%)

48 (48%)

102 (51%)

Mean ± SD

38.02 ± 6.43

38.34 ± 8.5

38.18 ± 7.52

0.764

t test;0.3

Median(IQR)

38(35-42)

38 (34.75-42)

38(35-42)

Range

22-53

21-64

21-64

LDL(mg/dL)

Normal

59 (59%)

78 (78%)

137 (68.50%)

0.004

Chi square test,8.365

Deranged

41 (41%)

22 (22%)

63 (31.50%)

Mean ± SD

118.86 ± 40.58

103.97 ± 36.34

111.42 ± 39.14

0.006

t test;2.733

Median(IQR)

118.5(82-141)

100 (76-125.25)

102(80.75-138)

Range

56-240

49-190

49-240

Triglyceride(mg/dL)

Normal

71(71%)

60 (60%)

131 (65.50%)

0.102

Chi square test,2.677

Deranged

29 (29%)

40 (40%)

69 (34.50%)

Mean ± SD

161.02 ± 81.55

152.15 ± 48.6

156.58 ± 67.1

0.597

Mann Whitney test;4784

Median(IQR)

135.5 (118-208.5)

144.5 (124.5-186)

140 (119.5-189)

Range

42-431

67-260

42-431

Table 3

Association of locality with diabetic retinopathy

Locality

Diabetic retinopathy(n=100)

No diabetic retinopathy(n=100)

Total

P value

Test performed

Rural

12 (12%)

48 (48%)

60 (30%)

<.0001

Chi square test,30.857

Urban

88 (88%)

52 (52%)

140 (70%)

Total

100 (100%)

100 (100%)

200 (100%)

Table 4

Association of occupation with diabetic retinopathy

Occupation

Diabetic retinopathy(n=100)

No diabetic retinopathy(n=100)

Total

P value

Test performed

Astrologer

0 (0%)

1 (1%)

1 (0.50%)

0.004

Fisher Exact test

Clerk

10 (10%)

4 (4%)

14 (7%)

Electrician

1 (1%)

0 (0%)

1 (0.50%)

Farmer

13 (13%)

32 (32%)

45 (22.50%)

Homemaker

52 (52%)

34 (34%)

86 (43%)

Plumber

1 (1%)

4 (4%)

5 (2.50%)

Retired clerk

3 (3%)

0 (0%)

3 (1.50%)

Retired mechanic

1 (1%)

0 (0%)

1 (0.50%)

Retired welder

2 (2%)

6 (6%)

8 (4%)

Shop owner

8 (8%)

9 (9%)

17 (8.50%)

Teacher

6 (6%)

7 (7%)

13 (6.50%)

Vendor

3 (3%)

3 (3%)

6 (3%)

Total

100 (100%)

100 (100%)

200 (100%)

Table 5

Association of education status with diabetic retinopathy

Education status

Diabetic retinopathy(n=100)

No diabetic retinopathy(n=100)

Total

P value

Test performed

No formal education

20 (20%)

43 (43%)

63 (31.50%)

0.007

Chi square test,14.201

Primary school

16 (16%)

9 (9%)

25 (12.50%)

Middle school

20 (20%)

20 (20%)

40 (20%)

High school

28 (28%)

16 (16%)

44 (22%)

College

16 (16%)

12 (12%)

28 (14%)

Total

100 (100%)

100 (100%)

200 (100%)

Discussion

In present study, out of 200 patients, 151 patients had dyslipidemia and 76 patients had diabetic retinopathy with dyslipidemia. The prevalence of dyslipidemia was found to be as high as 75.50% (Table 1). High prevalence of dyslipidemia has also been reported by Parikh et al.,9 who found the prevalence of dyslipidemia (the parameters used were: triglycerides above 150 mg/dl or LDL-C equal to or more than 100 mg/dl or HDL-C less than 40 mg/dl for males and less than 50 mg/dl among females) in diabetics (n=788) to be 97.8% in females and 85.5% in males. In another study by Joshi SR et al., 13.9% subjects were found to have raised total cholesterol, 29.5% of subjects had elevated triglyceride levels, 72.3% of subjects had reduced levels of HDL cholesterol, 11.8% of subjects had raised levels of LDL cholesterol and 79% of subjects had one of the lipid abnormalities.10

In our study, mean ± SD of LDL(mg/dL) in patients with diabetic retinopathy was 118.86 ± 40.58 which was significantly higher as compared to patients without diabetic retinopathy (Table 2) indicating a significant association of LDL(mg/dL) with diabetic retinopathy. (p value=0.006). This can be corroborated with the 1996, ETDRS report no. 22, which evaluated the relationship between serum lipid levels and retinal hard exudates in 2709 patients with diabetic retinopathy. At baseline, patients who were found to have elevated serum total cholesterol or elevated serum low-density lipoprotein cholesterol (LDL-C) levels were more likely to have retinal hard exudate.11

In our study, no significant association was seen in the distribution of total cholesterol (mg/dL), HDL(mg/dL), Triglyceride(mg/dL) with diabetic retinopathy (p value>.05)(Table 2)

Similar results were seen in a meta-analysis of 7 studies conducted by Yue Zhou et al., where obvious differences in TG, TC and HDL-C levels between patients with diabetic retinopathy and those without diabetic retinopathy were not found. However, slightly higher LDL-C levels were observed in the DR cases and in their study, Fenofibrate was proven to be beneficial in patients with DR and dyslipidemia.12 In a study by Idiculla J et al., 13 retinal hard exudate formation was found to have a positive statistical correlation with the presence of dyslipidemia (p=0.02), increased levels of total cholesterol (p=0.002) and also LDL levels (p=0.001).

In our study, significant association was found in the distribution of locality with diabetic retinopathy (p value<.05). 88% of patients with diabetic retinopathy (Table 3) resided in urban areas. This was significantly higher as compared to patients without diabetic retinopathy (52% resided in urban areas). These findings were similar to a study conducted in Chennai, India, where DR prevalence was observed to be 18% in urban areas.14 compared to 10.8 % in rural areas.15 This could be due to differences in the diet in urban areas and patients succumbing to diabetes related complications in rural areas due to difficulty in accessing better healthcare facilities. However, in a study conducted in China, DR prevalence in urban areas (18.1%) was much lower than in rural areas (29.1–43.1%).16, 17

Significant association was seen in the relationship of occupation with the presence of diabetic retinopathy in our study (p value<.05). 10% of patients with DR worked as clerks while 52% were homemakers (Table 4). This was significantly higher as compared to patients without diabetic retinopathy (4%, 34% respectively). 32% of patients without diabetic retinopathy were farmers compared to 13% of patients with diabetic retinopathy.

One prior study found that people working in sales, people engaged in manual work and unemployed individuals or housewives were screened less frequently for DR. However, the frequency of screening for DN was not affected by the occupation of the patient.18

In our study, significant association was seen between the education status of the patients and the occurrence of diabetic retinopathy (p value<.05). 16% of patients with DR had studied up to primary school while 28% of patients with DR had studied up/to high school(Table 5). This was significantly higher as compared to patients without diabetic retinopathy (9%, 16% respectively). On the other hand, 43% of patients without DR had no formal education which was significantly higher than patients with diabetic retinopathy (20%). Many previous studies18, 19, 20, 21 have confirmed that lower educational levels reduce frequency of DN and DR screening which could be due to lack of awareness and inability to understand the seriousness and the consequences of the complications of diabetes and due to lack of support and resources.

Conclusion

Various systemic risk factors have been studied and linked to diabetic retinopathy. Serum lipid levels seem to play a salient role in the progression of diabetic retinopathy. Significant association was seen in the distribution of LDL cholesterol in patients with diabetic retinopathy.

Clerks and homemakers were more predisposed to diabetic retinopathy. Subjects who were educated up to primary school and high school and subjects living in urban areas had significantly increased rates of diabetic retinopathy.

Source of Funding

None.

Conflict of Interest

The authors declare that there is no conflict of interest

References

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S H Byun S H Ma J K Jun K W Jung B Park Screening for diabetic retinopathy and nephropathy in patients with diabetes: a nationwide survey in KoreaPLoS One20138562991

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T H Rim I H Byun H S Kim S Y Lee J S Yoon Factors associated with diabetic retinopathy and nephropathy screening in Korea: the Third and Fourth Korea National Health and Nutrition Examination Survey (KNHANES III and IV)J Korean Med Sci201328681420

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© This is an open access article distributed under the terms of the Creative Commons Attribution License (creativecommons.org) which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


Article type

Original Article


Article page

218-223


Authors Details

Namratha Judith Cardoza, O K Radhakrishnan, Chaitali Desai, Kavitha Mohankumar, Madhuvanthi Mohan


Article History

Received : 04-12-2020

Accepted : 15-12-2020

Available online : 02-04-2021


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