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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 60  |  Issue : 4  |  Page : 294-300

Association of intraocular pressure with blood sugar levels in patients of type 2 diabetes mellitus and control group


1 Department of Ophthalmology, Government Doon Medical College, Dehradun, Uttarakhand, India
2 Department of Ophthalmology, Heritage Institute of Medical Sceinces, Varanasi, Uttar Pradesh, India

Date of Submission09-Apr-2022
Date of Decision21-Jul-2022
Date of Acceptance15-Aug-2022
Date of Web Publication19-Dec-2022

Correspondence Address:
Sushil Ojha
Government Doon Medical College Dehradun, Uttarakhand
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/tjosr.tjosr_38_22

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  Abstract 


Introduction: Glaucoma is a progressive optic neuropathy associated with loss of retinal ganglion cells, visual field loss and may or may not be associated with raised intraocular pressure (IOP). Although glaucoma is a multifactorial disease, elevated IOP remains the only modifiable risk factor. The direct relationship between IOP increase and decrease in retinal nerve fiber layer thickness has already been established by various authors previously. Hence, it is imperative to control the IOP to prevent the optic nerve damage and progressive visual field loss. The IOP can be influenced by various systemic factors, viz., hypertension, atherosclerotic diseases, body mass index (BMI), and diabetes mellitus (DM). Methodology: This study was conducted in a tertiary care center located in hilly areas of Northern India. Patients were recruited from out patient department (OPD).
Design: Prospective, cross-sectional and case-control study.
Sample: Patients attending medicine and ophthalmology OPD in Government Doon Medical College Hospital, Dehradun, were included in the study. Subjects were recruited as per selection criteria. This study included 25 patients with type 2 DM and 25 patients with the control group.
Inclusion criteria (Group 1:Diabetic patients):

  • Patients with diagnosed type 2 DM.

Inclusion criteria (Group 2: Non-diabetic patients):
  • Healthy subjects without any history of raised blood sugar levels in the last 2 years.

Exclusion criteria:
  • Diagnosed cases of glaucoma,
  • Diagnosed ocular hypertension,
  • Patients with corneal opacity, posterior segment diseases, or non-cooperative for eye examination,
  • Refractive error greater than ± 5D spherical, or cylindrical refractive error greater than ± 2.5D.

Capillary glucose testing:
IOP assessment: Immediately after the capillary glucose testing, IOP was measured in both eyes (i.e., fasting for exactly 10 hour and exactly 2 after breakfast) of each patient by Goldmann applanation tonometry.
All readings were taken with the patient in a sitting position.
Statistical analysis:All statistical analyses were performed with Statistical Package for Social Sciences version 21.0. Conclusion: We can conclude a significant relationship between glucose variation and IOP variation in the diabetic group with our results. The diabetic group exhibited higher values of fasting and post-prandial measurements than the control group. Hence, we recommend blood glucose testing in diabetic patients with glaucoma simultaneously with IOP monitoring. It should also include good blood sugar control. Though we are limited by a small sample size and time limit. A longitudinal study will help to get better and clearer results.

Keywords: Diabetes, primary open-angle glaucoma, prospective study


How to cite this article:
Ojha S, Kukreja P, Verma S. Association of intraocular pressure with blood sugar levels in patients of type 2 diabetes mellitus and control group. TNOA J Ophthalmic Sci Res 2022;60:294-300

How to cite this URL:
Ojha S, Kukreja P, Verma S. Association of intraocular pressure with blood sugar levels in patients of type 2 diabetes mellitus and control group. TNOA J Ophthalmic Sci Res [serial online] 2022 [cited 2023 Feb 3];60:294-300. Available from: https://www.tnoajosr.com/text.asp?2022/60/4/294/364245




  Introduction Top


Glaucoma is a progressive optic neuropathy associated with loss of retinal ganglion cells, visual field loss and may or may not be associated with raised intraocular pressure (IOP). Although glaucoma is a multifactorial disease, elevated IOP remains the only modifiable risk factor.[1],[2],[3],[4] The direct relationship between IOP increase and decrease in retinal nerve fiber layer thickness has already been established by various authors previously.[1],[2],[5],[6],[7] Hence, it is imperative to control the IOP to prevent the optic nerve damage and progressive visual field loss. The IOP can be influenced by various systemic factors, viz., hypertension,[8],[9],[10] atherosclerotic diseases,[8] body mass index (BMI),[11] and diabetes mellitus (DM).[8],[12],[13]

Although glaucoma is the second leading cause of blindness worldwide, it still remains a diagnostic challenge for clinicians as most of the patients are asymptomatic even up to the stage of advanced optic nerve damage and irreversible advanced visual field defects.[14]

According to various clinical studies, diabetes is associated with an increase in IOP[8],[15],[16],[17],[18],[19],[20],[21],[22],[23] and increased risk of developing open-angle glaucoma.[2],[24] An epidemiological study by Cho et al.[25] reported that there were 72 million people in India affected with DM in 2017 and were expected to increase up to 134 million by 2045 which surely is an exponential rise in the diabetic population. Clinicians in near future are going to encounter a large diabetic population with glaucoma. The only modifiable risk factor for glaucoma management is IOP, therefore, a better understanding of how variations in glucose levels can affect IOP would surely give additional information to the IOP assessment and management.

There is a lack of data regarding the distribution and the effect of factors influencing IOP in Indian population group, particularly from Uttarakhand State, which prompted us to take up this study. In this study, we aimed to determine whether fasting and post-prandial (PP) blood glucose levels among type 2 DM patients have any association with the fluctuations in their IOP when compared with the non-diabetics (control group).


  Review of Literature Top


Glaucoma is a blinding condition that may or may not be associated with high IOP.

In the year 1997, Mitchel et al.[13] in their perspective article, “Open-angle Glaucoma and Diabetes: The Blue Mountains Eye Study, Australia,” documented that glaucoma prevalence was higher in diabetic patients compared to those without diabetes [5.5% versus 2.8%, Odds ratio (OR) = 2.12].[12] Despite earlier conflicting opinions, a meta-analysis in 2015 by Di Zhao et al.[23] that included 47 studies from PubMed and EMBASE databases yielded a pooled relative risk of 1.48 for glaucoma in diabetic patients compared with non-diabetic patients. In a 10-year follow-up population-based cohort study by Czudowska et al. in 2010[26] to explore the influence of risk factors for open-angle glaucoma, ocular hypertension was found most important factor.

Oshitari et al.[27] and colleagues investigated the effect of chronic hyperglycemia on IOP in patients with DM and concluded that chronic hyperglycemia is associated with increased IOP in diabetic patients. Here, they divided the diabetic group into further three subgroups; diabetes with mild hyperglycemia [glycosylated hemoglobin A1c (HbA1c) ≤6.5%], moderate hyperglycemia (6.5% < HbA1c <8.0), and severe hyperglycemia (HbA1c ≥8.0%).

However, Pimentel et al.[28] in 2014 tested fasting blood sugar, PP blood sugar by capillary glucose testing and fasting IOP, PP IOP by Goldmann applanation tonometer in both diabetic and non-diabetic subjects and found increased IOP in PP state in both the groups. Yildiz et al. and others conducted a similar study like Pimentel et al. where PP blood sugar and PP IOP were tested after 75g of glucose intake by participants in both groups[29] and found that after an oral glucose tolerance test (OGTT), there was a rise in IOP in both the groups.

Lee et al. reported the relationship between IOP and systemic disorders and found that increased mean blood pressure is strongly correlated with the risk of increased IOP. Hence, it is pertinent to know if people with hypertensive participants are prone to high IOP.


  Aims and Objectives Top


  1. To explore whether there is any association between blood glucose levels (fasting and PP) and IOP values in diabetic patients and non-diabetics (control group).
  2. To find any difference in IOP in fasting and PP state among diabetic patients and non-diabetics (control group).
  3. To find the association of age, gender, and various risk factors (BMI, hypertension, smoking) on IOP among the patient group as well as a control group.



  Methodology Top


This study was conducted in a tertiary care center located in hilly areas of Northern India. Patients were recruited from out patient department (OPD). Before the sample collection, the approval from the Institutional Ethics Committee (IEC) was obtained. Informed written consent was obtained from each patient after a complete description of the study and handing over the patient information sheet.

Design: Prospective, cross-sectional and case-control study.

Sample: Patients attending medicine and ophthalmology OPD in Government Doon Medical College Hospital, Dehradun, were included in the study. Subjects were recruited as per selection criteria. This study included 25 patients with type 2 DM and 25 patients with control group.

Inclusion criteria (Group 1:Diabetic patients):

  • Patients with diagnosed type 2 DM.


Inclusion criteria (Group 2: Non-Diabetic patients):

  • Healthy subjects without any history of raised blood sugar levels in the last 2 years.


Hypertensive subjects in both groups were those with self-reported hypertension treated by antihypertensive medications.

All participants underwent a complete ophthalmological examination including a review of medical history, best-corrected visual acuity, slit-lamp bio-microscopy, IOP measurement, gonioscopy, and stereoscopic dilated fundoscopic examination with 90D. All ophthalmic examinations were done by an experienced ophthalmologist.

Exclusion criteria:

  • Diagnosed cases of glaucoma,
  • Diagnosed ocular hypertension,
  • Patients with corneal opacity, posterior segment diseases, or non-cooperative for an eye examination,
  • Refractive error greater than ± 5D spherical, or cylindrical refractive error greater than ± 2.5D.


Capillary glucose testing: All participants underwent capillary glucose testing in two distinct situations: first, baseline measurements (fasting for exactly 10 h, i.e., after overnight fasting) and, second, PP measurements (exactly 2 h after the meal, i.e., after breakfast). The same examiner performed all measurements without knowing the group of the patient (Masked). The measurement of capillary glucose was performed by collecting blood from the patient's left ring finger. After cleaning the finger tip with a spirit swab, it was allowed to air dry and thereafter pierced through the skin by a lancet and checked with an automated device (Contour Blood Glucose Meter, Bayer Polychem (India) Limited Diabetes Care Division).

IOP assessment: Immediately after the capillary glucose testing, IOP was measured in both eyes (i.e., fasting for exactly 10 h and exactly 2 h after breakfast) of each patient by Goldmann applanation tonometry.

All readings were taken with the patient in a sitting position. The same examiner performed all IOP measurements in a masked fashion and a different examiner performed the glucose level measurements. Third person collected the data in excel sheet.

Statistical analysis: Descriptive statistics included mean and standard deviation values for normally distributed variables. We used skewness/kurtosis tests and histograms to check normality. Paired t test were used for comparison of values between each time point (baseline and PP). For variables whose distribution rejected normality, a non-parametric test (Wilcoxon Rank Sum Test) was done. Whenever both eyes were found eligible, the right eye was arbitrarily chosen for this analysis.

All statistical analyses were performed with Statistical Package for Social Sciences version 21.0.


  Observations and Results Top


Demographic Characteristics of Participants: A total of 50 participants (25 diabetic and 25 non-diabetic) were included. Mean age of non diabetic patients was 37.9 ± 14.8 years and non-diabetic participants was 55.04 ± 10.4 years (range 16–72 years). [Table 1] depicts the demographic details of all the study participants.
Table 1: Demographic details of the study participants

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Mean BMI in the non-diabetic and diabetic group is 22.6 ± 4.7 and 25.3 ± 3.1, respectively. It differs significantly between the two groups (P < 0.05) [Table 1].

Blood sugar and IOP variations in both Groups: In diabetic group, mean fasting glucose level (143.16 ± 54.91 mg/dl) and mean PP glucose (201.92 ± 82.44 mg/dl) exceeds that of control group (mean fasting glucose level = 90.40 ± 11.51 mg/dl; mean PP glucose level = 107.20 ± 19.79 mg/dl) [Table 2].
Table 2: Mean blood glucose levels and mean IOP values at different states in diabetic and non-diabetic groups

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Also, mean fasting IOP (14.84 ± 3.24 mm Hg) and mean PP IOP (16.04 ± 2.31 mm Hg) were higher in the diabetic group than the control group (mean fasting IOP = 12.72 ± 2.42 mm Hg; mean PP IOP = 12.96 ± 2.26 mm Hg). IOP variation (diabetic group = 1.20 ± 3.01; non-diabetic group = 0.24 ± 1.47) with changes in blood sugar (diabetic = 58.76 ± 54.02; non-diabetic = 16.80 ± 20.36) is more in diabetic group compared to control group [Table 2], [Figure 1].
Figure 1: Fasting and PP IOP in both diabetic and non-diabetic groups

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As expected, PP glucose was higher than fasting glucose in both groups (diabetic patients; mean glucose difference = 58.76 ± 54.02 mg/dl and non-diabetic patients; mean difference = 16.80 ± 20.36 mg/dl). Mean IOP variation was found to be comparatively higher in the diabetic group than in the control group (1.20 ± 3.01 mm Hg in the diabetic group versus 0.24 ± 1.47 mm Hg in the control group) and the finding was statistically significant [Table 3], [Figure 2].
Table 3: Change in mean glucose variation and mean IOP change in diabetic and non-diabetic groups. (*): P value obtained by Wilcoxon Signed Ranks Test

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Figure 2: (x-axis represents glucose variation; y-axis represents IOP difference; blue dots represent higher variation plots in IOP and blood glucose in diabetic participants when compared to the control group; orange dots)

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Effect of gender on glucose variation and IOP variation: Comparison of mean IOP variation in females and males showed no significant results in both diabetic and non-diabetic groups. In the diabetic group, females (16.73 ± 2.18 mm Hg) had higher mean PP IOP than males (15 ± 2.21 mm Hg) was not found to be statistically significant (P = 0.185) [Figure 3], [Table 4].
Table 4: Comparison of blood glucose levels and IOP in males and females in both groups

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Figure 3: Comparison of fasting IOP and PP IOP in male and female in both diabetic and control groups

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Effect of BMI on glucose variation and IOP variation: Though values of BMI vary significantly in the diabetic and non-diabetic groups (P < 0.05). We are unable to find any significant relationship between BMI and glucose variation or IOP changes, probably due to the small sample size.

Effect of hypertension on glucose variation and IOP variation: The effect of hypertension on glucose variation and IOP changes could not be justified in the present study probably due to the inclusion of study participants with good control of Blood Pressure or due to the small sample size.


  Discussion Top


In our study, we performed fasting blood glucose level, fasting IOP and PP glucose level, PP IOP in 50 patients (25 diabetic and 25 non-diabetic), and IOP was found to be increasing with increasing blood glucose level in both groups. A mean increase of 1.20 mm Hg was observed in diabetic patients (P-value < 0.05), while there was an insignificant increase in non-diabetics.

The prevalence of DM is increasing all over the world and is one of the most common Global medical health problems.[31] The prevalence of DM increases with age. The glaucoma prevalence also increases with increasing age particularly primary open-angle glaucoma.[28] So, we will come across more patients with both diseases DM and Glaucoma together. But presently there is the dearth of literature available from Uttarakhand regarding patients having both medical conditions together.

For instance, Mitchel et al., Klein et al., and Dielemans et al. determined significant correlations between DM and glaucoma.[13],[20],[29] Zhao et al.[23] conducted a large sample size meta-analysis on a comparison of diabetic with non-diabetic participants, relative ratio for glaucoma was found to be 1.48 (95% CI, 1.29–1.76).

The association between DM and IOP has been documented in previous studies.[13],[15],[29] Wu and Leske[30] in the Barbados eye study stated diabetes, among other factors such as systolic blood pressure and age, was positively correlated with higher IOP values.[15] We believe that our results indirectly reflect the findings of Wu and Leske, although they did not evaluate the association between different state of blood sugar (fasting and PP) and IOP (at fasting and PP state). [Table 5] depicts the comparison of our findings with other studies.
Table 5: Comparison of our study with similar other studies based on the relationship between glucose and IOP measurements

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In spite of the paucity of studies correlating IOP changes with glucose variation, a variation positive relationship between IOP changes and glucose variation was found by Pimental et al. They conducted a study that included 37 patients (20 diabetic and 17 non-diabetic) and documented IOP increase of 2.3 mm Hg in diabetic and 1.6 mm Hg in non-diabetic patients.[31] Similarly, present study that included 50 participants (25 diabetic patients and 25 non-diabetic patients) noted statistically significant results in the diabetic group in IOP variation (1.2 mm Hg rise in diabetic versus 0.24 mm Hg rise in non-diabetics) with fasting and PP blood sugar, but Pimental et al. noted significant variation in both groups. So, we recommend IOP testing at different state of blood sugar only in diabetic patients.

Yildiz et al.[32] tried to find out the relation between blood sugar difference and IOP variation but with the inclusion of OGTT. In their perspective study including 51 patients (27 diabetic and 24 non-diabetic), they observed that the non-diabetic group exhibited IOPs within the normal range and a significant increase in IOP (in the right eye) that paralleled the blood glucose elevation, particularly within the first hour of the OGTT (P = 0.017). The diabetic group exhibited a significant increase in IOP (right and left eye) and was in parallel to the rise in blood glucose levels, more so in the first hour of the OGTT (P = 0.017 and P < 0.001 for right and left eye, respectively). This study supports our inference of IOP variation with different levels of blood sugar.

Our study differs from above-mentioned studies since we additionally evaluated the effect of gender, BMI, and hypertension, though not found statistically significant (P-value > 0.05).

Regarding the mechanism underlying the IOP changes with glucose variation, many propositions have been proposed. Lane et al.[33] stated that fluid flow is decreased by 15% in patients with type 1 diabetes without any evidence of microvascular complications when compared with healthy control participants.

We documented higher IOP variation in patients with more glucose difference, a mechanism for which is supported by studies mentioned in further discussion. Sato and Roy[34] suggested that high glucose levels may affect IOP by inducing an increase in fibronectin expression and cell proliferation in trabecular meshwork cells in the eye. Another suggested mechanism is an osmotic gradient created by hyperglycemia that draws excess aqueous humor into the anterior chamber of the eye.[35]

On the contrary, diabetic patients were reported to have higher central corneal thickness and lower corneal hysteresis, which may account for higher IOP in them.[36],[37]

From the clinical point of view, a large number of diabetic patients visit ophthalmology OPD on daily basis. Though some of them already suffer from glaucoma (ocular hypertension), many others can be saved from this permanent blindness if regular screening is undertaken. It is seen that for most of the diabetic patients, IOP measurement is considered important but blood sugar level is rarely assessed.

Our research successfully proved the relationship between blood glucose difference and IOP variation in diabetic patients, with a mean IOP increase of 8% (along with 41% increase in mean blood sugar level). Hence, there should be multiple measurements of blood sugar and IOP in patients with DM and glaucoma at regular time intervals.

Starting with limitations, firstly we are limited to a small sample size. With a larger sample size effect of gender, BMI, and hypertension could be found in diabetic and non-diabetic groups. Secondly, we have excluded glaucomatous diabetic subjects from our study, hence, influence of blood sugar variation (PP—fasting sugar) on intraocular variation (PP IOP—fasting IOP) cannot be documented in glaucomatous diabetic individuals. Also, we tested blood sugar levels by peripheral capillary glucose test which is good only for the self-use of the patient. Lastly, we did not measure central corneal thickness which can also affect IOP.


  Conclusion Top


We can conclude a significant relationship between glucose variation and IOP variation in diabetic group with our results. Diabetic group exhibited higher values of fasting and PP measurements than the control group. Hence, we recommend blood glucose testing in diabetic patients with glaucoma simultaneously with IOP monitoring. It should also include good blood sugar control.

Though, we are limited by a small sample size and time limit. A longitudinal study will help to get better and clearer results.


  Summary in Short and Understandable Top


Purpose: This is entirely a comparative study for IOP between the group of patients with type 2 DM and control group. We aimed to explore whether there is any association between blood glucose levels and IOP values in diabetic patients.

Description: We performed a study including 50 patients (25 diabetic and 25 non-diabetic), they underwent fasting (overnight, i.e., 8 h) and PP (2 h after a meal) blood glucose measurement by peripheral capillary glucose testing along with fasting and PP assessment of IOP by Goldmann applanation tonometer. All participants went under complete ophthalmic examination before inclusion in the study.

Results: As expected, PP glucose was higher than fasting glucose in both groups (diabetic patients; mean glucose difference = 58.76 ± 54.02 mg/dl and non-diabetic patients; mean difference = 16.80 ± 20.36 mg/dl). Mean fasting IOP (14.84 ± 3.24 mm Hg) and mean PP IOP (16.04 ± 2.31 mm Hg) were higher in diabetic group than control group (mean fasting IOP = 12.72 ± 2.42 mm Hg; mean PP IOP = 12.96 ± 2.26 mm Hg). Mean IOP variation was found to be significantly higher in the diabetic group (1.20 ± 3.01 versus 0.24 ± 1.47). Considering the P values (<0.05), the relationship between mean blood glucose variation and mean IOP variation was found to be statistically significant in the diabetic group.

Conclusion: We can conclude a significant relationship between glucose variation and IOP variation in the diabetic group with our results. The diabetic group exhibited higher values of fasting and PP measurements than the control group. Hence, we recommend blood glucose testing in diabetic patients with glaucoma simultaneously with IOP monitoring. It should also include good blood sugar control.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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    Tables

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