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 Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 30  |  Issue : 2  |  Page : 517-524

Comparisonbetweencorneal biomechanics and HbA1c levels in healthy individuals and type2 diabetic patients


1 Department of Ophthalmology, Menoufia University, Menoufia, Egypt
2 Research Institute of Ophthalmology, Giza, Egypt

Date of Submission21-Aug-2016
Date of Acceptance13-Nov-2016
Date of Web Publication25-Sep-2017

Correspondence Address:
Mahmoud E El Bahnasy
ElBahnasy, El-Abour, Kalubia, 12511
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.215460

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  Abstract 

Objectives
The aim of this study was to evaluate the corneal biomechanical properties using the ocular response analyzer(ORA) in type2 diabetic patients.
Background
The ORA isadevice developed in recent years and reveals the biomechanical properties of the cornea. It reflects certain biomechanical properties of the cornea, such as corneal hysteresis and corneal resistance factor.
Patients and methods
A total of150eyes of 75patients were enrolled in a cross-sectional prospective comparative study from May 2015 to May 2016. Patients were divided into three equal groups. ORA and HbA1c evaluation were carried out for all patients.
Results
The corneal hysteresis of the study groups ranged from 5.5 to 9.8mmHg for the control group (groupA), and it ranged from 6.00 to 11.4mmHg for the diabetic group(groupB), whereas it ranged from 9.5 to 15.20 in the diabetic group(groupC). The corneal resistance factor of the study groups ranged from 5.8 to 10.00mmHg for the control group(groupA), from 6.2 to 12.00mmHg for the diabetic group(groupB), and from 8.90 to 16.10mmHg for the diabetic group(groupC). The Goldmann-correlated intraocular pressure of our study groups ranged from 10 to 30mmHg for the control group(groupA), from 10 to 22mmHg for the diabetic group(groupB), and from 10.5 to 26.00mmHg for the diabetic group(groupC). The corneal-compensated intraocular pressure of the study groups ranged from 10.8 to 25mmHg for the control group(groupA), from 11.2 to 30mmHg for the diabetic group(groupB), and from 10.00 to 28.00mmHg for the diabetic group(groupC).
Conclusion
The corneal biomechanics in diabetic groups are significantly higher than those in the control group.

Keywords: cornea, corneal-compensated intraocular pressure, corneal hysteresis, corneal resistance factor, diabetes mellitus, Goldmann-correlated intraocular pressure, intraocular pressure


How to cite this article:
Elmazara HM, Mandour SS, El Bahnasy ME. Comparisonbetweencorneal biomechanics and HbA1c levels in healthy individuals and type2 diabetic patients. Menoufia Med J 2017;30:517-24

How to cite this URL:
Elmazara HM, Mandour SS, El Bahnasy ME. Comparisonbetweencorneal biomechanics and HbA1c levels in healthy individuals and type2 diabetic patients. Menoufia Med J [serial online] 2017 [cited 2019 Sep 15];30:517-24. Available from: http://www.mmj.eg.net/text.asp?2017/30/2/517/215460


  Introduction Top


Type2 diabetes mellitus is a systemic disorder affecting the eyes in many different forms and it is characterized by hyperglycemia[1].

Diabetic patients have a higher risk for epithelium healing problems, functional disorders of the corneal endothelium, and permanent stromal edema after intraocular surgical procedures[2].

Many studies have shown that diabetes is commonly associated with thicker corneas, and thus, in many diabetic patients, changes in the structure of the cornea are present[3].

The ocular response analyzer(ORA) is a device developed in recent years and reveals the biomechanical properties of the cornea. It reflects certain biomechanical properties of the cornea, such as corneal hysteresis (CH), corneal resistance factor(CRF), Goldmann-correlated intraocular pressure measurement (IOPg), and corneal-compensated intraocular pressure (IOPcc). CH gives an idea about the viscosity of the cornea; thus, it reflects the changes in the corneal stromal collagen organization. CH is not affected by the central corneal thickness. The ability to measure this effect is the key to understanding the biomechanical properties of the cornea and their influence on the intraocular pressure measurement process.

CRF readings showing the elastic properties of the cornea are partially independent of intraocular pressure but have a strong relationship with central corneal thickness. CH and CRF are good indicators to identify the biomechanical properties of the cornea[4].

Glycosylated hemoglobin(HbA1c) is the metabolic product of a stable connection of glucose to the N-terminal valine of the β-chain of hemoglobin. It defines the average blood glucose level of the preceding 3months and shows the result of diabetes treatment. Normally, the average HbA1c level varies between 4 and 6.4%. Higher values are a sign of insufficient blood glucose control and poor metabolic control.

An HbA1c target of 7.0% for the treatment of diabetes is generally accepted to lower the risk for long-term microvascular or macrovascular diabetes complications[5].


  Patients and Methods Top


A total of 150 eyesof 75patients were enrolled in our study. Patients were selected from ophthalmology outpatient clinics in Giza Research Institute for Ophthalmic Researches. Our study is a cross-sectional prospective comparative one. The study was carried out from May 2015 to May 2016. Patients were divided into three equal groups:

GroupA: This group included 50 eyes of age-matched normal individuals

GroupB: This group included 50 eyes of patients having diabetes mellitus type2 with HbA1c less than 7

GroupC: This group included 50 eyes of patients having diabetes mellitus type2 with HbA1c greater than 7.

Inclusion criteria

  • Presence of type2 diabetes mellitus
  • Normal fundus.


Exclusion criteria

History of ocular surgery.

History of refractive surgery.

Presence of systemic diseases other than diabetes mellitus that affects corneal biomechanics.

Presence of collagen diseases such as rheumatoid or lupus erythromatous.

Presence of corneal diseases or dystrophy.

Presence of keratoconus or suspicion of keratoconus.

Presence of glaucoma or suspicion of glaucoma.

Pseudoexfoliation syndrome.

Use of contact lenses.

Patient's evaluation

We planned to evaluate the effect of diabetes mellitus on the corneal biomechanics.

All patients underwent the following:

Full history taking with special emphasis on the following:

  • Age
  • Duration of diabetes
  • Diabetic control status
  • History of previous ocular surgeries.


Complete ophthalmic examination as follows:

  • Pupillary reaction
  • Visual acuity measurement: Uncorrected visual acuity and best-corrected visual acuity were measured using a Snellen chart
  • Anterior segment examination using slit-lamp examination
  • Fundus examination using+90 D lens (biomicroscopy) after pupillary dilatation with tropicamide 1% eye drops
  • Patients with a suspicion of corneal disorder such as early keratoconus were examined by a cornea specialist in our department, and corneal topography measurements were performed to exclude any form of keratoconus.


Investigations were carried out in the form of ORA (Reichert Technologies, Depew, NewYork, USA) to measure CH, CRF, IOPg, and IOPcc.

Investigations were carried out to diagnose diabetic patients in the form of glycated hemoglobin evaluation (HbA1c).

All diabetic patients received a diagnosis of diabetes according to the most recent guidelines published by the American Diabetes Association(2004).

HbA1c

HbA1c was obtained by means of venous blood sampling. HbA1c is the product of a stable linkage of glucose to the N-terminal valine of the β-chain of hemoglobin. It defines the average blood glucose level of the previous 2–3months. It reflects the success of diabetes therapy. Thus, it is possible to assess the glucose metabolism of the body more objectively and in long-term compared with a blood glucose sample, which reflects only the current sugar level. Usually 4–6.4% of hemoglobin is glycosylated. Higher values are a sign of insufficient blood glucose control. It also has advanced our understanding of the association between glycemic control and long-term complications of diabetes.

The ocular response analyzer

The ORA is a noncontact tonometer with automated eye centration alignment. Participants were seated on a chair and instructed to place their foreheads on the headrest of the ORA device that was made to match their height by adjusting the height of a table.

To avoid startling the participants, they were first briefed about a noncontact probe that would move toward the eye and emit a sudden but gentle puff of air. Participants were told to focus on a blinking red light in the device.

Thereafter, the ORA was activated and the air puff was emitted onto the center of the cornea. The ORA readings were obtained consecutively and only good quality readings were stored. If poor-quality waveforms were obtained, they were deleted, and a new measurement was taken.

Only the readings with liability more than 7 were stored. The manufacturer defined good-quality readings as both force-in and force-out applanation signal peaks on the ORA waveform being fairly symmetrical in height. The ORA displayed a graphic representation of the corneal response after each measurement[Figure 1].
Figure 1: Ocular response analyzer (ORA) signals.

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[Figure2] and [Figure3] represent the ORA signals provided from our diabetic patients during our study.
Figure 2: Ocular response analyzer (ORA) signal of the right eye of patient number 14 of the diabetic group.

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Figure3: Ocular response analyzer (ORA) signal of the right eye of patient number 39 of the diabetic group.

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[Figure4] represents the ORA signal provided from a normal individual in normal group during our study.
Figure 4: Ocular response analyzer (ORA) signal of the right eye of patient number 11 of the normal group.

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The red curve is the 'dynamic map' of the cornea obtained during the rapid in/out deformation. That dynamic process generated two signal peaks that defined the two applanation states. The difference between these inward and outward motion applanation pressures (P1 and P2) was called CH.

The ORA software utilized the CH to generate two additional parameters: the IOPcc and the CRF. An IOPg was also provided by the machine.

Statistical analysis

The collected data of normal and diabetic patients were tabulated in spreadsheets using Microsoft Office Excel 2007 (Microsoft Corporation, Chicago, USA). The coded data were arranged for use in SPSS Statistical Computer Package (SPSS 2011, version20; IBM Corporation, USA). The first step in statistical analysis was to conduct descriptive statistics on the file containing the collected data of the 80patients. Descriptive data were summarized and presented herein for numerical data as the mean±SD. Categorical data(i.e.non-numerical data) are expressed in the percentage that each category represents in the whole sample.

Throughout the analysis, numerical data are considered normally distributed based on the results of the Kolmogorov–Smirnov test of normality using SPSS package.

The independent-samples t-test procedure was used to compare means for the two groups of cases–namely, normal and diabetic. As the patients of each group were randomly selected, any difference in response or measure is considered to be due to diabetes and not other factors.

The correlation between two different numerical variables was determined using bivariate correlation procedure, which computes Pearson's correlation coefficient(r) and its significance level. Throughout the statistical analysis, the results were considered statistically significant when the significance level or P value was 0.05 or less for two-tailed test.


  Results Top


A total of 150 eyes of 75patients were enrolled in our study. Patients were selected from ophthalmology outpatient clinics in Giza Research Institute for Ophthalmic Researches. Our study is a cross-sectional prospective comparative one. The study was carried out from May 2015 to May 2016.

The age of our study groups ranged from 34 to 71years, with an average of 54.93±9.02years for the control group(groupA), 58.50±6.38years for groupB, and 57.66±7.5years for groupC[Table1].
Table1: Age of the study groups (years)

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Our study included 71 eyes of male patients and 79 eyes of female patients(female eyes: male eyes ratio was 1:1.11). Thecontrol group(groupA) included 23male and 27female similar to the diabetic group (groupB), whereas groupC included 25male and 25female patients [Table 2].
Table 2: Sex distribution in both groups

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The HbA1c in our study ranged from 5 to 6.2% with an average of 5.663±0.33% in the control group(groupA), from 5 to 7% with an average of 6.42±0.432% in the diabetic group(groupB), and from 7 to 12.6% with an average of 7.2169% ±1.932[Table3].
Table 3: HbA1c of both groups (%)

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The spherical equivalent in our study ranged from−6.00 to+7.13 in decimals and with an average of−0.01±1.62 for the control group(groupA), from−8.00 to+3. 0 with an average of−0.79±3.02 for the diabetic group(groupB), and from−7.5 to 2.5 with an average of−0.528±2.24 in groupC[Table4].
Table 4: Spherical equivalent of the study groups

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The CH of the study groups ranged from 5.5 to 9.8mmHg with an average of 7.11±0.846mmHg for the control group(groupA). It ranged from 6.00 to 11.4mmHg, with an average of 8.295±1.091mmHg for the diabetic group(groupB). However, it ranged from 9.5 to 15.20 with an average of 11.299±1.178 for the diabetic group(groupC)[Table5].
Table 5: Corneal hysteresis of the study group (mmHg)

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The CRF of the study groups ranged from 5.8 to 10.00mmHg, with an average of 7.17±0.979mmHg for the control group(groupA), from 6.2 to 12.00mmHg, with an average of 8.6902±1.2519mmHg for the diabetic group(groupB), and from 8.90 to 16.10mmHg with an average of 11.8928±1.5419mmHg for the diabetic group(groupC)[Table6].
Table 6: Corneal resistance factor of the study groups (mmHg)

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  Discussion Top


The human cornea is a viscoelastic tissue that can be described by two principal properties:(a) a static resistance component(characterized by the CRF), for which deformation is proportional to applied force, and(b) a dynamic resistance component(characterized by CH), for which the relationship between deformation and applied force depends on time, both CH and the CRF are measured using a dynamic bidirectional applanation process using the ORA[6].

Diabetes significantly impacts the morphological, metabolic, physiological, and clinical properties of the cornea. Chronic hyperglycemia resulting from poorly controlled diabetes leads to tissue modifications and changes in the corneal structure. Glucose can act as a collagen cross-linking agent with the help of advanced glycation end products(AGEs)[7].

The presence of AGEs in tissues leads to an increase in collagen cross-linking that result in an impairment of tissue function. It is thought that increased collagen cross-linking in the corneas of diabetic patients results in gradual corneal stiffening, increased corneal thickening, and biomechanical changes. Therefore, the aim of our clinical study was to investigate whether the biomechanical parameters(CH and CRF) of the cornea are altered in diabetes according to the HbA1c level. To compare the metabolic status of diabetic and nondiabetic individuals, HbA1c was obtained.

Our population study was divided into three equal groups: groupA included 50 eyes of 25 normal individuals; groupB included 50 eyes of 25patients with diabetes mellitus type2 with HbA1c less than 7; and groupC included 50 eyes of 25patients with HbA1c greater than 7, providing a reference to establish the typical values and ranges of corneal biomechanical parameters.

In our study, the mean CH in the control group(groupA) was 7.1186±0.84660mmHg in comparison with the mean CH in the diabetic group(groupB), which was 8.2958±1.09100mmHg, and the mean CH in groupC, which was 11.2992±1.17842. It was statistically significantly higher in diabetic patients when compared with the control group and was statistically significantly higher in groupC diabetic patients(P=0.00).

Our results could be attributed to increased glucose in diabetes that acts as a collagen cross-linking agent with the help of AGEs. AGEs accumulate in collagen proteins, resulting in the formation of covalent cross-linking bonds and gradual corneal stiffening.

Kotecha etal. [8] mentioned in their results that CH is slightly higher in diabetic eyes(P=0.21).

In contrast, Sahin etal. [7] reported that the mean CH in the control group was 10.41±1.66mmHg in comparison with the mean CH in the diabetic group, which was 9.51±1.82mmHg. He also reported that the mean CH was significantly lower in diabetic patients when compared with the control group(P=0.0001). He attributed the decrease in CH to an alteration in the collagenous components due to collagen cross-linking, suggesting that the dampening effects of the cornea decrease because of diabetes and were induced to increase during the cross-linking of collagen fibrils.

Meanwhile, Goldich etal. [9], Hager etal. [10], and Cankaya etal. [11] disagreed with our results as they noted that there was no statistically significant difference between the control and diabetic groups as regards CH values. They did not provide any explanations. In the study by Cankaya etal. [11], the mean CH in the control group was 9.41±0.5mmHg and the mean CH in the diabetic group was 9.44±0.62mmHg(P=0.738).

Scheler etal. [12] also disagreed with our results as he showed that there were no differences detected between healthy controls and patients with well-controlled diabetes as regards CH. He reported that the diabetic changes caused by increased glucose levels with a consecutive formation of AGEs seemed not to be surprising in a group of patients with diabetes who had a normal HbA1c.

The hypothesis of Scheler etal. [12] was confirmed by the studies by Odetti etal. [13] and Traverso etal. [14], as they reported that insulin may reduce or exaggerate the effect of diabetes, which he showed in insulin-dependent patients with diabetes.

Scheler etal. [12] also noted that CH was higher in poorly controlled diabetic patients than in the control group.

In our study, the mean CRF value of the control group (groupA) was 7.1731±0.97952mmHg in comparison with 8.6902±1.25195mmHg in the diabetic group (groupB) and 11.8928±1.54254 in groupC. The difference between the three groups was significantly higher in diabetic patients and more significantly higher in groupC (the diabetic group) (P=0.001).

There were previous studies that showed similar results to ours, such as the studies by Goldich etal. [9] and Kotecha etal. [8], who reported a P value of 0.001. They did not provide any explanation.

Cankaya etal. [11] also showed similar results to ours as they reported that the mean CRF in the control group was 10.56±0.5mmHg in comparison with 11.58±0.6mmHg in the diabetic group. They also reported that the difference between the control and diabetic groups was statistically significantly higher in the diabetic group compared with the control group(P<0.01), but they did not explain this finding.

In contrast, Sahin etal. [7] did not agree with our results. They denoted that there were no statistically significant differences between the control and diabetic groups(P=0.8) and the mean CRF in the control group was 10.36±1.97mmHg and the mean CH in the diabetic group was 10.32±1.76mmHg. They could not find an exact explanation for their finding, but it matched the findings of Scheler and colleagues(30).

Scheler etal. [12] also did not agree with our results, as he mentioned that there were no differences detected between healthy controls and patients with well-controlled diabetes as regards CRF. However, there were statistically significantly higher differences comparing the control group with the poorly controlled diabetic group.

In our study, we wanted to investigate whether the biomechanical parameters(CH and CRF) of the cornea were altered in diabetes and whether they are affected by diabetic control; we correlated CH and CRF with HbA1c.

As regards CH and duration of diabetes in the diabetic group(groupB), the correlation was a weak positive linear correlation(r=0.273; P=0.089).

As regards CH and HbA1c, in the control group (groupA) there was almost no correlation between the two (r=0.005; P=0.974), but in the diabetic group(groupB) there was a weak positive linear correlation(r=0.129; P=0.427).

This elevation in HbA1c leading to a slightly increased CH indicate an increase in the viscosity of the ground substance. The increased viscosity is associated with higher corneal shearing strength and increased damping. This increased damping effect, which is reflected in a higher CH, is most likely due to the glycosylation of proteoglycans and glycosaminoglycans(the Maillard reaction) with a consecutive formation of AGE.

Diabetes reduces the washout of proteoglycans and glycosaminoglycans, as they are connected strongly among each other compared with nondiabetic patients. This 'fixation' of the glycosaminoglycans can change the biomechanical properties of the cornea by increasing the damping capacity.

However, Sahin etal. [7] disagreed with us as they reported that neither HbA1c nor disease duration had any statistically significant effect on CH(P>0.05).

Kotecha etal. [8] disagreed with our results as they confirmed the findings of Sahin etal. [7]. Sahin etal. [7] proposed that there was no association between CH and HbA1c(r=0.1; P=0.44).

However, Kotecha etal. [8] agreed with our results in having a positive association between duration of diabetes and CH(r=0.16; P=0.23). They reported that a longer duration of diabetes was associated with a greater CH, although this trend did not achieve significance.

Del Buey etal. [15] disagreed with our results as they proposed that CH is significantly influenced by the viscosity of the ground substance and a decrease in viscosity leads to a decrease in CH.

As regards CRF and duration of diabetes in the diabetic group(groupB), the correlation revealed a weak positive linear correlation(r=0.237; P=0.141).

As regards CH and HbA1c, in the control group(groupA) there was almost no correlation between the two(r = −0.092; P=0.570). However, in the diabetic group(groupB) there was a moderate positive linear correlation(r=0.353; P=0.025).

However, Sahin etal. [7] disagreed with our results as they reported that neither HbA1c nor disease duration had any statistically significant effect on CRF(P>0.05).

Moreover, Kotecha etal. [8] disagreed with our results as they found no correlation between CFR and HbA1c(r=0.07; P=0.60) and no correlation was found between CRF and duration of diabetes(r=0.11; P=0.39).

Kotecha etal. [8] proposed that CRF is strongly associated with corneal stiffness.

In our study, the mean HbA1c in the control group (groupA) was 5.6366±0.33186% and 6.4262±0.43890% in the diabetic group(groupB) and 9.5880±1.44443% in the diabetic group(groupC).

Kotecha etal. [8] reported that the mean HbA1c for the diabetic group was 7.2±1.4%(P=0.69).

Sahin etal. [7] also proposed that the mean HbA1c in the diabetic group was 7.31±1.53%.

Scheler etal. [12] proposed that the mean HbA1c was 5.44±0.46% in the control group, 6.00±0.78% in the diabetic group1, and 8.58±2.44% in the diabetic group2. Group1 had HbA1c less than 7% and group2 had HbA1c of at least 7%; HbA1c was statistically significantly different between the control group and all patients with diabetes(groups1+2)(P=0.0001).

In our study, the duration of diabetes was 10.48±5.39years in the diabetic group(groupB), whereas Sahin etal. [7] proposed that the mean diabetes duration in their study group was 13.5±6.3years.


  Conclusion Top


The corneal biomechanics in diabetic groups are significantly higher compared with those of the control group, as the mean CH is 9.6±1.89mmHg in the control group(groupA) and 11.29±2mmHg in the diabetic group(groupB). The difference in CH between the three groups is statistically highly significant(P=0.00). Meanwhile, the mean CRF is 9.48±1.745mmHg in the control group(groupA) and 11±2.29mmHg in the diabetic group(groupB) and the difference in CRF between the two groups is statistically highly significant(P=0.001). In the control group, there is no correlation between CH and the average level of HbA1c(r=0.005; P=0.974). However, there is a weak positive linear correlation between CH and the average level of HbA1c in the diabetic patients(r=0.129; P=0.427). There is a very weak negative linear correlation between CRF and the average level of HbA1c in the control group(r = −0.092; P=0.570). However, the correlation between it and HbA1c in the diabetic group is a moderate positive linear correlation(r=0.237; P=0.141).

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Aiello LM, Cavallerano JD: Ocular complications of diabetes mellitus. In: editors, Kahn CR, Weir GC. Joslin's diabetes mellitus. 13thed. Philadelphia: Lea and Febiger; 1994. 771–793.  Back to cited text no. 1
    
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Goebbels M, Spitznas M. Endothelial barrier function after phacoemulsification: a comparison between diabetic and nondiabetic patients. Graefes Arch Clin Exp Ophthalmol 1991; 229:254–257.  Back to cited text no. 2
    
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Larsson LI, Bourne WM, Pach JM, Brubaker RF. Structure and function of the corneal endothelium in diabetes mellitus typeI and typeII. Arch Ophthalmol 1996; 114:9–14.  Back to cited text no. 3
    
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Chihara E. Assessment of true intraocular pressure: the gap between theory and practical data. Surv Ophthalmol 2008; 53:203–218.  Back to cited text no. 4
    
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Laakso M, Cederberg H. Glucose control in diabetes: which target level to aim for? J Intern Med 2012; 272:1–12.  Back to cited text no. 5
    
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Dupps WJJr, Wilson SE. Biomechanics and wound healing in the cornea. Exp Eye Res 2006; 83:709–720.  Back to cited text no. 6
    
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Sahin A, Bayer A, Özge G, Mumcuoglu T. Corneal biomechanical changes in diabetes mellitus and their influence on intraocular pressure measurements. Invest Ophthalmol Vis Sci 2009; 50:4597–5604.  Back to cited text no. 7
    
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Kotecha A, Oddone F, Sinapis C, Elsheikh A, Sinapis D, Sinapis A, etal. Corneal biomechanical characteristics in patients with diabetes mellitus. JCataract Refract Surg 2010; 36:1822–1828.  Back to cited text no. 8
    
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Goldich Y, Barkana Y, Gerber Y, Rasko A, Morad Y, Hasrstein M, etal. Effect of diabetes mellitus on biomechanical parameters of the cornea. JCataract Refract Surg 2009; 35:715–719  Back to cited text no. 9
    
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Hager A, Wegscheider K, Wiegand W. Changes of extracellular matrix of the cornea in diabetes mellitus. Graefes Arch Clin Exp Ophthalmol 2009; 247:1369–1374.  Back to cited text no. 10
    
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Cankaya C, Gunduz E, Doganay S, Ulutaz O. Corneal biomechanical characteristics, intraocular pressure and central corneal thickness in patients with type2 diabetes mellitus. J Clin Med Res 2012; 4:79–83.  Back to cited text no. 11
    
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Scheler A, Spoerl E, Boehm AG. Effect of diabetes mellitus on corneal biomechanics and measurement of intraocular pressure. Acta Ophthalmologica 2012; 90:e447–e451.  Back to cited text no. 12
    
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Odetti P, Traverso N, Cosso L, Noberasco G, Pronzato MA, Marinari UM. Good glycaemic control reduces oxidation and glycation end-products in collagen of diabetic rats. Diabetologia 1996; 39:1440–1447.  Back to cited text no. 13
    
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Traverso N, Odetti P, Pronzano MA, Marinari UM, Cottalasso D. Intensive insulin treatment reduces the accumulation of oxidation and glycation end-products in diabetic rat collagen. Aging(Milano) 1997; 9:432–433.  Back to cited text no. 14
    
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Del Buey MA, Cristobal JA, Ascaso FJ, Lavilla L, Lanchares E. Biomechanical properties of the cornea in Fuchs' corneal dystrophy. Invest Ophthalmol Vis Sci 2009; 50:3199–3202.  Back to cited text no. 15
    


    Figures

  [Figure 1], [Figure2], [Figure3], [Figure4]
 
 
    Tables

  [Table1], [Table 2], [Table3], [Table4], [Table5], [Table6]



 

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