• Users Online: 374
  • Print this page
  • Email this page


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 60  |  Issue : 1  |  Page : 23-29

Prospective clinical study of ocular manifestations in patients with type 2 diabetes mellitus


Department of Ophthalmology, Shri Nijalingappa Medical College and Hanagal Shri Kumareshwar Hospital and Research Centre, Bagalkot, Karnataka, India

Date of Submission07-Oct-2021
Date of Decision07-Dec-2021
Date of Acceptance15-Dec-2021
Date of Web Publication22-Mar-2022

Correspondence Address:
Dr. Shilpa Umarani
Department of Ophthalmology, Shri Nijalingappa Medical College and Hanagal Shri Kumareshwar Hospital and Research Centre, Bagalkot, Karnataka
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/tjosr.tjosr_153_21

Rights and Permissions
  Abstract 


Purpose: The purpose of this study is to determine the common ocular manifestations in diabetes and their relation to the duration and severity of the diabetes. Methodology: This is a prospective, observational study of patients attending the outpatient department and those referred to the tertiary eye care hospital in Bagalkote district of Karnataka from October 2012 to March 2014. Type 2 diabetic patients were recruited on the basis of history, clinical examination, and blood investigations. Along with detailed demographic history, all participants underwent complete slit-lamp anterior segment, posterior segment examination and intraocular pressure measurement was done. Estimation of random blood sugar at admission and fasting blood sugar and postprandial blood sugar second day of admission along with urine sugar, albumin, and microscopy. If necessary based on the indication, fundus fluorescein angiography was also performed. Results: Out of 350 patients evaluated, 211 were male (60.3%) and 139 (39.7%) were female. Diabetic retinopathy (DR) was the most common complication (36.8%), followed by cataract 35.4%, glaucoma (4.6%), and other pathologies such as conjunctivitis, recurrent hordeolum, and dacrocystitis. The strongest predictor for the prevalence of retinopathy in persons with Type 2 diabetes is the duration of diabetes and was proven statistically significant. Both prevalence and severity of retinopathy correlate with HBA1C level in our study group. The most common type of cataract found was cortical type (41.2%) followed by senile posterior cortical (29.8%). Diabetes predisposes to infection in different body parts, and ocular structures are not an exception. Conclusion: DR was the most common ocular complication of diabetes, followed by cataract and primary open angle glaucoma. The prevalence and severity of DR were higher in patients with the longer duration of diabetes.

Keywords: Cataract, diabetes, diabetic retinopathy, ocular complications


How to cite this article:
Umarani S, Dollaiah A, Vallabha K. Prospective clinical study of ocular manifestations in patients with type 2 diabetes mellitus. TNOA J Ophthalmic Sci Res 2022;60:23-9

How to cite this URL:
Umarani S, Dollaiah A, Vallabha K. Prospective clinical study of ocular manifestations in patients with type 2 diabetes mellitus. TNOA J Ophthalmic Sci Res [serial online] 2022 [cited 2022 Jun 29];60:23-9. Available from: https://www.tnoajosr.com/text.asp?2022/60/1/23/340357




  Introduction Top


Diabetes mellitus has progressed from a pathology affecting primarily people in developed countries into a true worldwide epidemic in the last few decade.[1] In 1999, the World Health Organization gave the definition of diabetes mellitus as “a metabolic syndrome with multiple etiologies, characterized by chronic hyperglycemic state along with disturbances of carbohydrate, fat, and protein metabolism resulting from defects in insulin secretion, action, or both.”[2] Uncontrolled diabetes mellitus can manifests as long-term damage, dysfunction and failure of various organs, resulting in microvascular and macrovascular complications.[2] It was estimated that in 2005 approximately 200 million people had diabetes mellitus globally. Most of these patients are classified as having Type 2 diabetes mellitus and the metabolic syndrome.[3] As per the global statistics, about 300 million people are expected to have diabetes by 2025, affecting approximately 5.4% of the world's population.[3] Changing dietary and exercise trends tend to play a leading role in the increasing prevalence of diabetes mellitus. It is unfortunate that India is known as the Diabetes Capital of the World. A decade back, India reported 62.4 million people with Type 2 diabetes, compared to 50.8 million the previous year, according to the International Diabetes Federation and the Madras Diabetes Research Foundation. India now tops with the prevalence of diabetes about 9%. By 2030, India will have 100 million people with diabetes.[4] Diabetes mellitus being a lifestyle disease is on the rise in urban areas; Shankar Netralaya reported that the prevalence of diabetes mellitus in the population older than 40 years, in urban India, was around 28% in 2014.[5]

Diabetic retinopathy (DR) is the commonly ocular sequalae of uncontrolled diabetes and the most common cause of blindness among people 20–64 years of age in the U. S.[6],[7] It is also the 6th most common cause of blindness in India National Program for Control of Blindness.[7] A meta-analysis by Yau et al.[8] estimated that among individuals with diabetes, the overall prevalence of any DR was 34.6%, proliferative DR (PDR) was 7.0%, diabetic macular edema was 6.8%, and vision-threatening DR was 10.2%. The Chennai Urban Rural Epidemiology Eye Study from South India reported the prevalence of DR about 17.6%, significantly lower than age-matched western counterparts.[9] Detailed literature analysis reveals that diabetic complications can be reduced with strict glucose control. It has been seen that intensive blood glucose control alleviates the risk of developing retinopathy by 54%. Neuropathy was reduced by 60% and albuminuria by 54%, respectively.[10] With regard to Type 2 diabetes mellitus, the United Kingdom Prospective Diabetes Study showed a 21% reduction in risk for progression of DR over a 12-year period in the intensive group.[11] Skyler et al. have demonstrated that HBA1C levels correlate in a direct relationship with the relative risk of diabetic microvascular complications.[12] Strict glucose control, weight control, and exercise remain the essential elements to prevent the complications of diabetic disease.[13]

The burden of blindness due to DR can be ameliorated by intervening at early stages of DR.[14] With the available cost-effective methods of early screening, appropriate strategies/models need to be developed.[14] The National Program for Control of Blindness of India suggests opportunistic screening for the early identification of DR.[15] It is the responsibility of ophthalmology community to create awareness in the society to prevent these complications and to treat them promptly. It is in this context, we have studied the prevalence of diabetic eye complications at our tertiary eye care hospital in Bagalkote district of Karnataka. As per the best of our knowledge and as per the detailed literature, none of the previous studies have high studied the prevalence and distribution of ocular problems among Type 2 diabetics in Bagalkote district of Karnataka.


  Methodology Top


This was a prospective observational study of patients attending the outpatient department and those referred to the department of ophthalmology at a tertiary care hospital in South India from October 2012 to March 31, 2014. The study adhered to the tenets of Declaration of Helsinki. The study approval was obtained from the Institutional Review Board of the Institutional Ethics Committee and informed consent was obtained from all the study participants. All Type 2 diabetes patients were recruited on the basis of history, clinical examination, and blood investigations. Patients were labeled as Type 2 diabetes mellitus based on the criteria laid down by the American Diabetes Association. All participants were interviewed as per the prepared pro forma and the complete slit lamp anterior segment, posterior segment examination using + 90D lens and slit lamp biomicroscope, and indirect ophthalmoscope with + 20D lens and corneal sensations were assessed using a wisp of cotton on slit lamp with the patient looking in the opposite gaze. Intraocular pressure measurement (indentation tonometer) was done. Applanation tonometry and gonioscopy were done as and when required. Visual field analysis was done using Humphrey perimetry and optical coherence tomography was done whenever needed. Estimation of random blood sugar, fasting blood sugar, and postprandial blood sugar along with urine sugar, albumin, and microscopy were done on the same day. If necessary based on the indication fundus fluorescein angiography was also performed in required participants. All the patients were admitted for a detailed comprehensive evaluation. The inclusion criteria were (a) patients who have been diagnosed Type 2 diabetes mellitus and (b) patients more than 30 years of age. The following patients were excluded from the study: (a) patient with Type 1 diabetes, (b) patients with known eye disease not related to diabetes, (c) systemically unfit patients will other known comorbidities, and (d) patients requiring hospital admission due to any other reason. Data obtained in the study were analyzed statistically using the SPSS for Windows version 23.0 software. The continuous variables were stated as median (minimum-maximum) values and categorical variables as number (n) and percentage (%). In the analysis of categorical variables, the Chi-square test was used, and Spearman's rho analysis was applied to determine the correlations between the categorical data. The Mann–Whitney U-test was applied to continuous variables. A value of P < 0.05 was accepted as statistically significant in all the analyses.


  Results Top


A total of 350 patients of noninsulin-dependent diabetes mellitus were analyzed. Out of 350, 211 were males (60.3%) and 139 (39.7%) were females [Table 1]a. Among both the sexes, the age groups between 51 and 60 years had the maximum number of patients (33.7%) [Table 1]a. Among the ocular complications-related diabetes, the most common was involvement of retina: 142 patients (40.6%) followed by the lens 124 (35.4%) [Table 1]b. We observed that all the anatomical parts of eye are involved in diabetes. Forty-three patients had some eyelid lesions, of which 14 had Hordeolum and another 14 had Xanthelasma, 13 had Blepharitis and 2 had recurrent chalazion [Table 1]c. The conjunctival lesions found were pterygium in 19 patients (5.4%) and infective conjunctivitis in 6 patients (1.7%). A total of 7 patients had corneal ulceration (2%), 3 had reduced corneal sensation (0.9%) while 1 patient (0.3%) had a corneal perforation. The corneal sensations were assessed using a wisp of cotton on slit lamp with the patient looking in the opposite gaze. Four out of these 7 ulcers were nonhealing bacterial corneal ulcers. For intraocular pressure (IOP) measurement, majority had IOP between 10 and 15 mm Hg (63%), whereas 21 (6%) of them had more 21 mm Hg. These findings are statistically significant (P < 0.001), which means the presence of intraocular hypertension in this population is having a positive association with Type 2 diabetes [Table 2]a. Nine patients (2.7%) were diagnosed with primary open angle glaucoma (POAG). Eight patients (2.3%) had neovascular glaucoma. One hundred and twenty-four of the total patients had presented with cataract (35.4%) which makes it the second most common mode of ocular diabetic disease in our study. Most common variant found was cortical: 51 of them (41.2%) in the study which is more prevalent than the 39 posterior cortical (31.4%), 28 also had nuclear cataract (29.8%). Six had mature cataract (4.8%), whereas 4 (3.2%) had the characteristic snow flake appearing cataract [Table 2]b. It clearly shows that most of the people develop any one of these cataracts in the age group of 51–70 years (70.9%). The finding has been confirmed by statistical significant P = 0.008. Nine patients had vitreous hemorrhage at presentation (2.6%), whereas 9 patients had asteroid hyalosis. A total of 129 patients were affected by some form of retinopathy (36.8%) making it the most common pathological condition. 114 of them (32.6%) had non-PDR (NPDR) while 15 had PDR (4.3%). In the NPDR group, 33 of them had mild NPDR (25.6%), 51 had moderate (39.5%) and 30 had severe NPDR (23.5%) [Table 3]a. Eighteen of these patients had Caricom Single Market and Economy (CSME) (5.6%). In this study, most of the patients were in 51–60 years' (33%) age group. The average age of the patients studied was 50.9 years. A significant association was found between age group and retinal complication of diabetes mellitus (P = 0.001) [Table 3]b. In the present study 211 patients were male while 139 patients were female. Of these, 111 men and 55 women were affected by some kind of retinal disease [Table 4]a and [Figure 1]. We found significant association between sex and ocular complication of diabetes mellitus (P < 0.001) wherein both mild NPDR and severe NPDR were more common in males than in females. Our study showed no difference in the prevalence of PDR in either sexes (9% each), while slightly more common CSME in men (11.7%) than in females (9.1%). The prevalence of combined retinal lesions was more common in males (211, 52.6%) than females (120, 39.6%). 11.7% of people are affected by mild NPDR within 5 years of Type 2 diabetes, which increases significantly to 23.7% and 25% by 10 years and thereafter [Table 4]b. Similarly, moderate NPDR rises from 25% to 28.9% and 36.8% in same interval. The severe NPDR type prevalence rises from 8.3% to 18.8% within 5 years to more than 10 years of diabetes. Furthermore, PDR prevalence increased from 1.7% to 13.2% [Figure 2]. From [Table No 5]a, it is clear that 16.1%, 65.8%, and 95.5% prevalence was observed for HBA1C of 6%–7%, 7%–8%, and >8%, respectively. It is also seen that the mild NPDR (87.9%) is found clustering at lower levels of HBA1c (<8%), moderate NPDR (68.6%) is most prevalent between 7% and 8% of HBA1C levels and severe NPDR (73.3%) is most common at >8% levels. 250 of our patients (i.e., 65.1%) were taking regular treatment, while 90 (34.9%) of them were not regular with their medications. Apparently, 60.6% of mild NPDR patients were on regular treatment than 39.3% who were not [Table 5]b. The P value of this is 0.964, which indicates dissociation between the two. Other retinal lesions such as age-related macular degeneration (ARMD) was present in 4 of them, central retinal vein occlusion, branch retinal artery occlusion (BRAO), central retinal artery occlusion, and retinal detachment in 2 each, while 1 patient had branch retinal vein occlusion (BRVO). Two of the patients had optic nerve atrophy, whereas 1 had an acute inflammation. There were three patients with isolated 3rd cranial nerve palsy, whereas another patient one had 6th nerve palsy with no other neurological deficits.


Click here to view


Click here to view


Click here to view


Click here to view


Click here to view
Figure 1: Distribution of retinopathy patients according to sex

Click here to view
Figure 2: Co-relation between HBA1C levels and prevalence of retinopathy

Click here to view



  Discussion Top


In this study, most of the patients were found to be in the age group of 51–60 years. Comparable age distribution was found in the Wisconsin epidemiologic study of DR.[16] The average duration of diabetes in the study group was 6.4 years in males and 7.3 years in females. In the present study, we found that retinal lesions were the most common ocular complication occurring in diabetes subjects (40.6%), of which retinopathies of all kind constituted majority of them (36.8%). The prevalence of cataract was 35.4% followed by glaucoma (4.6%) and other ocular pathologies such as conjunctivitis, recurrent hordeolum, and dacrocystitis. Stanga et al.[17] in their review of literature in 1999 have found that retinopathy is the most common ocular complication of long-standing diabetes mellitus followed by other lesions such as cataract, uveitis, and neuro-ophthalmitis. It is generally recognized in the existing literature that retinopathy is the most common ocular complication in Type 2 diabetes. Our study confirms that DR in its various forms is the most common complication of diabetic eye disease in India.

Different eye lid lesions were noted in our study such as recurrent stye (4%), xanthelasma (4%), blepharitis (3.7%), and recurrent chalazion (0.6%). Xanthelasma is rare in the general population. Variable incidence of 0.56%–1.5% has been reported from the western developed nations.[18] The incidence in our study is 4%, which is explained by the fact that xanthelasma is a cutaneous marker for underlying diabetes and dyslipidemia.

Diabetes predisposes to infection in different body parts, and ocular structures are not any different from it. Thus, recurrent styes (4%), blepharitis (3.7%), conjunctivitis (1.7%), and dacrocystitis (2.6%) can be explained in our group of patients. Kruse have confirmed in their case control study that diabetes is a risk factor for acute infectious conjunctivitis, with an odds' ratio of 1.24 in diabetics.[19]

There were 19 patients with Pterygium in our study group, which makes it 5.42% prevalence. In contrast, two different studies, one by Asokan, (Chennai group, 2012)[20] and Zhong[21] (study of adult Chinese population) have statistically found out no association between prevalence of pterygium and diabetes.

Microbial keratitis is a vision-threatening entity and is one of the major causes of blindness globally. Diabetic patients with microbial keratitis are at an increased risk than nondiabetics and require immediate medical treatment to prevent irreversible sequalae. There were seven patients with corneal ulcer of which 5 were bacterial type and 1 was nonhealing. There was 1 patient presenting with corneal perforation. This signifies the need for appropriate microbiological diagnosis of microbial corneal ulceration to provide prompt and effective medical remedy and to avoid empirical treatment.

Nielsen found that the prevalence rate of POAG and ocular hypertension was 6.0% and 3.0%, respectively, in diabetes Type 2 patients. Neovascular glaucoma occurred in 2.3% of all diabetics.[22] In our study, we had 21 patients, i.e., 6% with ocular hypertension (IOP >21 mmHg), 8 patients (2.3%) were of neovascular type and rest being POAG (2.6%). Thus, the prevalence is similar in both studies. Nearly two thirds of the Indian diabetic population showed evidence of cataract; mixed cataracts were more common than the monotypes ones in a recent study by Raman et al.[23] 35.4% of our study population had cataract which is lesser than the Shankar Netralaya group [Table 2]c. Twenty patients in our group had mixed type of cataracts (14.7%) which is lesser than the total number of monotypes. The most common type of cataract found was cortical type (41.2%) followed by senile posterior cortical (29.8%). The characteristic snow flake cataract of diabetes is found in only 3.2% of cataract patients, which is of similar lower incidence in many studies. We operated on all patients with visual acuity of <6/36, 2 patients had posterior capsular opacity, 1 had conjunctivitis, and rest did not have any major problems. We infer that cataract surgery in diabetes is safe and good results can be expected as in any other group. Studies have reported that the prevalence of DR in India varies from 20% to 31%. The Aravind Eye Disease Survey in Southern India reported a retinopathy prevalence of 27% in a population aged 30 years or older with self-reported diabetes,[24] similar to the 22% prevalence reported from another population-based study in an urban population in Hyderabad, India.[25] The prevalence of retinopathy in our study population was 36.8%, of which NPDR was 32.6% and PDR was 4.3%. In the younger onset group in the WESDR, the prevalence of any retinopathy was 8% among participants with diabetes duration of 3 years, 25% for 5 years, 60% for 10 years, and 80% for 15 years.[16] In the present study, the prevalence of proliferative retinopathy was 1.7% for those with diabetes duration of 5 years, increasing to 13.2% for 10 years. In our study, the prevalence of NPDR varied from 26.1% in persons who had diabetes for <5 years to 32.3% in persons who had diabetes for 5–10 or more years and 78.7% in more than 10 years. Increased incidence of CSME was noted as the duration of diabetes increased (11.7%–13.2% over the same duration intervals of diabetes.) Similar increased incidence of CSME with increased duration of diabetes was noted in a study by Klein R. et al.[26] The findings are thus consistent with the fact that the strongest predictor for the prevalence of retinopathy in persons with Type 2 diabetes is the duration of diabetes and was proven statistically significant (P < 0.002). The WESDR showed that both the younger-onset and older-onset patients with diabetes who had no retinopathy had significantly lower mean glycosylated hemoglobin values than those patients with retinopathy.[16] Patients with higher glycosylated hemoglobin values were shown to have a higher risk of retinopathy, such that those with mean HbA1c levels over 12% were 3.2 times more likely to have retinopathy after 4 years than subjects with HbA1c levels under 12%.[27] Our study population exhibits a similar pattern: 16.1% of diabetic patients with HBA1C between 6% and 7% had some form of DR, while the prevalence rises to 65.8% and 95.5% with HBA1C of 7%–8% and more than 8% (i.e., uncontrolled type), respectively. It is also seen that the mild NPDR is found clustering at lower levels of HBA1c (<7%), moderate NPDR is most prevalent between 7% and 8% of HBA1C levels and severe NPDR is most common at >8% levels. Thus, both prevalence and severity of retinopathy correlate with HBA1C level in our study group. In our study, participants taking regular treatment (oral tablets/ insulin) had a combined NPDR prevalence of 24% which is lower when compared to the group not taking treatment regularly (48.9%) [Figure 3]. The essentials for managing a diabetes mellitus patient are regular treatment and follow-up. In a study conducted by Jacobson et al.,[27] Rush JA showed that diabetes is the underlying cause in 25%–30% of patients aged 45 years and older who develop acute extraocular muscle palsy.[28] In a study by Watanabe et al., 1% of patients with diabetes was found to have cranial nerve palsies, compared with only 0.13% of controls.[29] 1.1% of our patients (i.e., 4 of them) had cranial nerve palsy, same as with the Watanabe et al. study. We found a prevalence of 0.3% BRVO among diabetics in our study, whereas BRVO was detected in 0.79% in a study conducted by Kawasaki.[30]
Figure 3: Severity of nonproliferative diabetic retinopathy versus regular and irregular treatment

Click here to view



  Conclusion Top


Retinal lesions (such as retinopathies, CSME, BRVO, BRAO, ARMD, and RD) were the most common ocular complication occurring in diabetes participants (40.6%), of which retinopathies of all kind constituted majority of them (36.8%). The prevalence of cataract was 35.4% followed by glaucoma (4.6%) and other ocular pathologies such as conjunctivitis, repeated styes, and dacrocystitis. Diabetes predisposes to infection in different body parts, and ocular structures are not an exception. Both prevalence and severity of retinopathy correlate with HBA1C level in our study group. Diabetic patients with microbial keratitis are at an increased risk than nondiabetic persons and require immediate medical attention.

Acknowledgment

The authors would like to thank Shri Nijalingappa Medical College and Hanagal Shri Kumareshwar Hospital and Research Center, Bagalkot, Karnataka, India.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care 1997;20:1183-97.  Back to cited text no. 1
    
2.
Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. National diabetes data group. Diabetes 1979;28:1039-57.  Back to cited text no. 2
    
3.
King H, Aubert RE, Herman WH. Global burden of diabetes, 1995-2025: Prevalence, numerical estimates, and projections. Diabetes Care 1998;21:1414-31.  Back to cited text no. 3
    
4.
Ramachandran A, Snehalatha C, Ma RC. Diabetes in South-East Asia: An update for 2013 for the IDF diabetes atlas. Diabetes Res Clin Pract 2014;103:231-7.  Back to cited text no. 4
    
5.
Rajiv R, Rani PK, Sudhir R. Prevalence of diabetic retinopathy in India sankara Nethralaya diabetic retinopathy epidemiology and molecular genetics study report 2. Ophthalmology 2009;116:311-8.  Back to cited text no. 5
    
6.
Cavallerano J. Ocular manifestations of diabetes mellitus. Optom Clin 1992;2:93-116.  Back to cited text no. 6
    
7.
Congdon NG, Friedman DS, Lietman T. Important causes of visual impairment in the world today. JAMA 2003;290:2057-60.  Back to cited text no. 7
    
8.
Yau JW, Rogers SL, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 2012;35:556-64.  Back to cited text no. 8
    
9.
Rema M, Premkumar S, Anitha B, Deepa R, Pradeepa R, Mohan V. Prevalence of diabetic retinopathy in urban India: The Chennai urban rural epidemiology study (CURES) eye Study, I. Invest Ophthalmol Vis Sci 2005;46:2328-33.  Back to cited text no. 9
    
10.
Nisar MU, Asad A, Waqas A, Ali N, Nisar A, Qayyum MA, et al. Association of diabetic neuropathy with duration of Type 2 diabetes and glycemic control. Cureus 2015;7:e302.  Back to cited text no. 10
    
11.
Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) group. Lancet 1998;352:837-53.  Back to cited text no. 11
    
12.
Skyler JS. Diabetic complications. The importance of glucose control. Endocrinol Metab Clin North Am 1996;25:243-54.  Back to cited text no. 12
    
13.
Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, et al. Exercise and Type 2 diabetes: The American College of Sports Medicine and The American Diabetes Association: Joint position statement. Diabetes Care 2010;33:e147-67.  Back to cited text no. 13
    
14.
Vashist P, Singh S, Gupta N, Saxena R. Role of early screening for diabetic retinopathy in patients with diabetes mellitus: An overview. Indian J Community Med 2011;36:247-52.  Back to cited text no. 14
[PUBMED]  [Full text]  
15.
Raman R, Ramasamy K, Rajalakshmi R, Sivaprasad S, Natarajan S. Diabetic retinopathy screening guidelines in India: All India ophthalmological society diabetic retinopathy task force and vitreoretinal society of India consensus statement. Indian J Ophthalmol 2021;69:678-88.  Back to cited text no. 15
[PUBMED]  [Full text]  
16.
Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin epidemiologic study of diabetic retinopathy. III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol 1984;102:527-32.  Back to cited text no. 16
    
17.
Stanga PE, Boyd SR, Hamilton AM. Ocular manifestations of diabetes mellitus. Curr Opin Ophthalmol 1999;10:483-9.  Back to cited text no. 17
    
18.
Jonson A, Sigfusson N. Letter: Significance of xanthelasma palpebrarum in the normal population. Lancet 1976;1:372.  Back to cited text no. 18
    
19.
Kruse A, Thomen RW. Diabetes and risk of acute infectious conjunctivitis-a population-based case-control study. Diabet Med 2006;23:393-7.  Back to cited text no. 19
    
20.
Asokan R, Venkatasubbu RS, Velumuri L, Lingam V, George R. Prevalence and associated factors for pterygium and pinguecula in a South Indian population. Ophthalmic Physiol Opt 2012;32:39-44.  Back to cited text no. 20
    
21.
Zhong H. Prevalence of and risk factors for pterygium in rural adult Chinese populations of the Bai nationality in Dali: The Yunnan minority eye study. Invest Ophthalmol Vis Sci 2012;53:6616-8.  Back to cited text no. 21
    
22.
Nielsen NV. The prevalence of glaucoma and ocular hypertension in Type 1 and 2 diabetes mellitus. An epidemiological study of diabetes mellitus on the island of Falster, Denmark. Acta Ophthalmol (Copenh) 1983;61:662-72.  Back to cited text no. 22
    
23.
Raman R. Pal SS, Adams JS. Prevalence and risk factors for cataract in diabetes: Sankara nethralaya diabetic retinopathy epidemiology and molecular genetics study, Report No. 17. Invest Ophthalmol Vis Sci 2010;51:6253-61.  Back to cited text no. 23
    
24.
Narendran V, John RK, Raghuram A, Ravindran RD, Nirmalan PK, Thulasiraj RD. Diabetic retinopathy among self reported diabetics in southern India: A population based assessment. Br J Ophthalmol 2002;86:1014-8.  Back to cited text no. 24
    
25.
Dandona L, Dandona R, Naduvilath TJ, McCarty CA, Rao GN. Population based assessment of diabetic retinopathy in an urban population in southern India. Br J Ophthalmol 1999;83:937-40.  Back to cited text no. 25
    
26.
Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. Glycosylated hemoglobin predicts the incidence and progression of diabetic retinopathy. JAMA 1988;260:2864-71.  Back to cited text no. 26
    
27.
Jacobson AM, Hauser ST, Willett J, Wolfsdorf JI, Herman L. Consequences of irregular versus continuous medical follow-up in children and adolescents with insulin-dependent diabetes mellitus. J Pediatr 1997;131:727-33.  Back to cited text no. 27
    
28.
Rush JA. Extra ocular muscle palsies in diabetes mellitus. Int Ophthalmol Clin 1984;24:155-9.  Back to cited text no. 28
    
29.
Watanabe K, Hagura R, Akanuma Y, Takasu T, Kajinuma H, Kuzuya N, et al. Characteristics of cranial nerve palsies in diabetic patients. Diabetes Res Clin Pract 1990;10:19-27.  Back to cited text no. 29
    
30.
Kawasaki R. The prevalence of diabetic retinopathy and other fundus diseases in Japanese population: 2nd year experience in Funagata, Japan. Invest Ophthalmol Vis Sci 2002;43:43-82.  Back to cited text no. 30
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Methodology
Results
Discussion
Conclusion
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed366    
    Printed18    
    Emailed0    
    PDF Downloaded33    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]