The Open Ophthalmology Journal




ISSN: 1874-3641 ― Volume 13, 2019
RESEARCH ARTICLE

Higher Intraocular Pressure Levels Associated With Lower Hysteresis In Type 2 Diabetes



Sinan Bekmez1, *, Tolga Kocaturk2
1 Department of Ophthalmology, Dr. Behcet Uz Children’s Training and Research Hospital, Izmir, Turkey
2 Department of Ophthalmology, Faculty of Medicine, Adnan Menderes University, Aydin, Turkey

Abstract

Aim:

To investigate the differences of corneal biomechanic characteristics using Ocular Response Analyzer (ORA, Reichert; USA) on type 2 diabetics and healthy subjects.

Methods:

One hundred eyes of 100 subjects (between the ages of 17-91) who applied to Adnan Menderes University’s Ophthalmology Clinic between January-March 2015 were included in this study, 50 diabetics (Group 1) and 50 healthy controls (Group 2). The eyes included in the study were randomly chosen. Corneal Hysteresis (CH), Corneal Resistance Factor (CRF), Goldmann correlated Intraocular Pressure (IOPg) and corneal compensated Intraocular Pressure (IOPcc) of patients were measured by ORA. Detailed ophthalmological examinations were done for every subject. Kolmogorov-Smirnov test was used to analyze the distribution of quantitative variables and t test was used for the data that were normally distributed. Any p value <0.05 was considered as statistically significant.

Results:

The mean ages were 63.3±9.0 and 61.7±11.6 in Group 1 and 2, respectively (p=0.459). 25 (50.0%) were female, 25 (50.0%) were male in Group 1 and 26 (52.0%) were female, 24 (48.0%) were male in Group 2 (p=1.000). Mean IOPcc values were 17.8±3.6 (12.1-29.0) and 16.0±3.1 (10.9-23.8) mmHg (p=0.006); mean IOPg values were 16.9±3.5 (10.9-25.9) and 15.4±2.9 (9.0-24.7) mmHg (p=0.032); mean CH values were 9.9±1.5 (6.1-13.3) and 10.5±1.7 (6.5-15.7) (p=0.080) and mean CRF values were 10.4±1.6 (7.5-14.0) and 10.5±1.7 (6.6-15.4) (p=0.730) in Groups 1 and 2, respectively.

Conclusions:

There was no any statistical difference between the groups in terms of CH and CRF. However, mean CH and CRF values were found less in diabetic group. Corneal biomechanical differences seen in diabetic patients may be associated with a statistically significantly higher IOP measurements.

Keywords: Ocular response analyzer, Corneal biomechanic properties, Type 2 diabetes mellitus, Corneal hysteresis, Intraocular pressure, Lower hysteresis.


Article Information


Identifiers and Pagination:

Year: 2018
Volume: 12
First Page: 29
Last Page: 33
Publisher Id: TOOPHTJ-12-29
DOI: 10.2174/1874364101812010029

Article History:

Received Date: 27/10/2017
Revision Received Date: 10/02/2018
Acceptance Date: 07/03/2018
Electronic publication date: 28/03/2018
Collection year: 2018

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© 2018 Bekmez and Kocaturk.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Department of Ophthalmology, Dr. Behcet Uz Children’s Training and Research Hospital, Izmir, Turkey, Tel: +905057572615; E-mail: sinanbekmez@gmail.com
There is no source of support in this study.





1. INTRODUCTION

Ocular Response Analyzer (ORA, Reichert; USA), which is a non-contact tonometer, is the first device capable of dynamic evaluation of the in vivo biomechanical properties of the cornea [1Luce DA. Determining in vivo biomechanical properties of the cornea with an ocular response analyzer. J Cataract Refract Surg 2005; 31(1): 156-62.[http://dx.doi.org/10.1016/j.jcrs.2004.10.044] [PMID: 15721708] ]. The device sprays the air jet to form deformation in the cornea. ORA air pressure creates two cornea current response measurements (P1, P2) depending on the impact: The force required to flatten the cornea with rising pressure, and the force required to flatten the cornea again with decreasing pressure. The difference between the two pressures (P1-P2) is termed “Corneal Hysteresis” (CH). The average of the two applanation pressure is described as compatible with Goldmann IOP (IOPg). The device taking into account the CH determines a second IOP (IOPcc), compensated by the biomechanical properties of the cornea. The other important parameter of the device is a Corneal Resistance Factor (CRF) [2Kotecha A. What biomechanical properties of the cornea are relevant for the clinician? Surv Ophthalmol 2007; 52(Suppl. 2): S109-14.[http://dx.doi.org/10.1016/j.survophthal.2007.08.004] [PMID: 17998034] ]. Clinical trials with ORA have shown that the device is not affected or slightly affected by CCT values [3Chihara E. Assessment of true intraocular pressure: The gap between theory and practical data. Surv Ophthalmol 2008; 53(3): 203-18.[http://dx.doi.org/10.1016/j.survophthal.2008.02.005] [PMID: 18501267] ].

Diabetes Mellitus (DM) is a systemic disease which affects the eye in very different ways: diabetic retinopathy, neovascular glaucoma, cataract, ptosis, oculomotorius nerve palsy [4Goebbels M. Tear secretion and tear film function in insulin dependent diabetics. Br J Ophthalmol 2000; 84(1): 19-21.[http://dx.doi.org/10.1136/bjo.84.1.19] [PMID: 10611093] ]. Dry eye symptoms can typically be observed in diabetics, like burning and foreign body sensation, decreased in visual quality [4Goebbels M. Tear secretion and tear film function in insulin dependent diabetics. Br J Ophthalmol 2000; 84(1): 19-21.[http://dx.doi.org/10.1136/bjo.84.1.19] [PMID: 10611093] ]. Besides corneal complications in diabetic patients, CCT was investigated. In some publications, there is no difference in CCT between diabetic patients and normal subjects [5Bron AM, Creuzot-Garcher C, Goudeau-Boutillon S, d’Athis P. Falsely elevated intraocular pressure due to increased central corneal thickness. Graefes Arch Clin Exp Ophthalmol 1999; 237(3): 220-4.[http://dx.doi.org/10.1007/s004170050222] [PMID: 10090585] , 6Inoue K, Kato S, Inoue Y, Amano S, Oshika T. The corneal endothelium and thickness in type II diabetes mellitus. Jpn J Ophthalmol 2002; 46(1): 65-9.[http://dx.doi.org/10.1016/S0021-5155(01)00458-0] [PMID: 11853716] ]. Many publications reported that CCT increased in diabetic patients [7Ravalico G, Tognetto D, Palomba M, Calderini S, Vattovani O. Corneal endothelial function in diabetes: A fluorophotometric study. Ophthalmologica 1994; 208(4): 179-84.[http://dx.doi.org/10.1159/000310482] [PMID: 7970543] -10Lee JS, Oum BS, Choi HY, Lee JE, Cho BM. Differences in corneal thickness and corneal endothelium related to duration in diabetes. Eye (Lond) 2006; 20(3): 315-8.[http://dx.doi.org/10.1038/sj.eye.6701868] [PMID: 15832184] ].

The aim of this study was to investigate the differences in corneal biomechanic characteristics between the patients with and without type 2 DM.

2. METHODS

One hundred eyes of 100 subjects (between the ages of 17-91) who applied to university outpatient clinic between January-March 2015 were included in this study, 50 diabetics (Group 1) and 50 controls (Group 2). The eyes included in the study were randomly chosen. CH, CRF, IOPg and IOPcc of patients were measured by ORA.

The patient exclusion criteria of the study include: patients who have any corneal pathology, uveitis, and posterior segment pathology, lens pathology that prevent the fundus examination, dry eye or conjunctivitis is detected, ocular trauma and previous ocular surgery history, patients who underwent ocular intravitreal injection, patients who take any topical treatment, patients who get treatment medications for systemic disease except DM and patients who noncooperate to measure with ORA.

The study protocol had the approval of the university’s ethics committee and complied with the guidelines set forth in the Declaration of Helsinki. Detailed ophthalmological examinations were done for every subject.

2.1. Statistical Analysis

Kolmogorov-Smirnov test was used to analyze the distribution of quantitative variables and t- test was used for the data that were normally distributed. Any p value <0.05 was considered as statistically significant. If the data did not fit a normal distribution, Mann-Whitney-U test was used for comparisons between the groups. Descriptive statistics of normally distributed data were shown as mean ± standard deviation. Descriptive statistics were shown as the median (25-75 percentiles) for the data that did not fit a normal distribution. Chi-square test was used for qualitative data analysis and descriptive statistics were shown as frequency (percent). All results were analyzed statistically using the SPSS (Statistical Package for the Social Sciences; SPSS Inc., Chicago, IL, USA) version 16 software package for Windows.

3. RESULTS

The mean ages were 63.3±9.0 and 61.7±11.6 in Group 1 and 2, respectively (p=0.459). 25 (50.0%) were female, 25 (50.0%) were male in Group 1 and 26 (52.0%) were female, 24 (48.0%) were male in Group 2 (p=1.000) (Table 1). Mean IOPcc values were 17.8±3.6 (12.1-29.0) and 16.0±3.1 (10.9-23.8) mmHg (p=0.006); mean IOPg values were 16.9±3.5 (10.9-25.9) and 15.4±2.9 (9.0-24.7) mmHg (p=0.032); mean CH values were 9.9±1.5 (6.1-13.3) and 10.5±1.7 (6.5-15.7) (p=0.080) and mean CRF values were 10.4±1.6 (7.5-14.0) and 10.5±1.7 (6.6-15.4) (p=0.730) in Groups 1 and 2, respectively (Table 2). There was no statistical difference between the groups in terms of CH and CRF. However, mean CH and CRF values were found less no in the diabetic group. There was a statistically significant difference between the diabetic and nondiabetic groups in terms of IOP parameters. Mean IOPcc and IOPg values were found high in the diabetic group.

Table 1
Demographics of Groups.


Table 2
Mean IOPcc, IOPg, CH and CRF values of the groups.


4. DISCUSSION

In our study, we investigated the differences of ORA measurements between healthy subjects and type 2 diabetic patients. Mean IOPcc and IOPg values were found to be statistically significantly high in the diabetic group, associated with lower CH and CRF levels.

The study of Scheler et al. investigated the relationship between HbA1c levels and ORA measurements in diabetic patients [11Scheler A, Spoerl E, Boehm AG. Effect of diabetes mellitus on corneal biomechanics and measurement of intraocular pressure. Acta Ophthalmol 2012; 90(6): e447-51.[http://dx.doi.org/10.1111/j.1755-3768.2012.02437.x] [PMID: 22691299] ]. They revealed a higher rate of CH and CRF levels in poorly controlled diabetic patients. There wasn't any difference between the well-controlled diabetic patients and healthy control groups in biomechanical measurements in their study.

In Cankaya et al.’s study, they compared the biomechanic properties of the cornea between patients with and without type 2 diabetes [12Cankaya C, Gunduz E, Doganay S, Ulutas O. Corneal biomechanical characteristics, intraocular pressure and central corneal thickness in patients with type 2 diabetes mellitus. J Clin Med Res 2012; 4(6): 79-83.]. IOPg, CRF and CCT values were statistically significantly higher in diabetic patients than healthy subjects. We revealed a higher rate of IOPcc and IOPg values in diabetic patients.

Corneal viscosity may affect CH measure. In previous studies, it has been shown to decrease CH with viscosity reduction [13del Buey MA, Cristóbal JA, Ascaso FJ, Lavilla L, Lanchares E. Biomechanical properties of the cornea in Fuchs’ corneal dystrophy. Invest Ophthalmol Vis Sci 2009; 50(7): 3199-202.[http://dx.doi.org/10.1167/iovs.08-3312] [PMID: 19255149] ]. Independent of other factors, increasing age can cause a decrease in viscosity [14Moreno-Montañés J, Maldonado MJ, García N, Mendiluce L, García-Gómez PJ, Seguí-Gómez M. Reproducibility and clinical relevance of the ocular response analyzer in nonoperated eyes: Corneal biomechanical and tonometric implications. Invest Ophthalmol Vis Sci 2008; 49(3): 968-74.[http://dx.doi.org/10.1167/iovs.07-0280] [PMID: 18326720] ].

The high rates IOP that we measured in DM patients compared to the control group may be an indication that diabetes affects corneal biomechanical measurements. As seen in other studies we have found that an inverse relationship between IOP and CH [15Bilen O, Akinici A, Ertan A. Corneal hysteresis and corneal resistance factor in diabetic patients with proliferative diabetic retinopathy: A controlled study XXVI Congress of ESCRS Berlin.2008., 16Hirneiss C, Neubauer AS, Yu A, Kampik A, Kernt M. Corneal biomechanics measured with the ocular response analyser in patients with unilateral open-angle glaucoma. Acta Ophthalmol 2011; 89(2): e189-92.[http://dx.doi.org/10.1111/j.1755-3768.2010.02093.x] [PMID: 21288308] ].

Some studies show that high IOP and glaucoma may develop in diabetic patients. Bonovas et al. suggest that diabetic patients are at significantly increased risk of developing primary open-angle glaucoma [17Bonovas S, Peponis V, Filioussi K. Diabetes mellitus as a risk factor for primary open-angle glaucoma: A meta-analysis. Diabet Med 2004; 21(6): 609-14.[http://dx.doi.org/10.1111/j.1464-5491.2004.01173.x] [PMID: 15154948] ].

In a study with using specular microscopy, chronic metabolic stress occurs as a result of hyperglycemia in diabetics and it can cause morphological changes in the corneal endothelium [18Schultz RO, Matsuda M, Yee RW, Edelhauser HF, Schultz KJ. Corneal endothelial changes in type I and type II diabetes mellitus. Am J Ophthalmol 1984; 98(4): 401-10.[http://dx.doi.org/10.1016/0002-9394(84)90120-X] [PMID: 6486211] ].

There are many publications which investigated the causes of the structural changes in the cornea in patients with diabetes. McNamara et al. suggest that hyperglycemia can affect water retention in the cornea and this situation can cause structural changes in the cornea [19McNamara NA, Brand RJ, Polse KA, Bourne WM. Corneal function during normal and high serum glucose levels in diabetes. Invest Ophthalmol Vis Sci 1998; 39(1): 3-17.[PMID: 9430539] ].

In a research, mean CCT and Goldmann applanation tonometry IOP, IOPcc, and IOPg were significantly higher in diabetic patients than in healthy control subjects [20Sahin A, Bayer A, Ozge G, Mumcuoglu T. Corneal biomechanical changes in diabetes mellitus and their influence on intraocular pressure measurements 2009.[http://dx.doi.org/10.1167/iovs.08-2763] ]. Similar results are observed in many studies [21Hennis A, Wu SY, Nemesure B, Leske MC. Hypertension, diabetes, and longitudinal changes in intraocular pressure. Ophthalmology 2003; 110(5): 908-14.[http://dx.doi.org/10.1016/S0161-6420(03)00075-7] [PMID: 12750088] , 22Dielemans I, de Jong PT, Stolk R, Vingerling JR, Grobbee DE, Hofman A. Primary open-angle glaucoma, intraocular pressure, and diabetes mellitus in the general elderly population. The Rotterdam Study. Ophthalmology 1996; 103(8): 1271-5.[http://dx.doi.org/10.1016/S0161-6420(96)30511-3] [PMID: 8764798] ].

Corneal biomechanical differences seen in diabetic patients may be associated with statistically significantly higher IOP measurements. Actually, we do not know “how and why” diabetes affects corneal biomechanical measurements. Further studies are needed to answer these questions. We may only speculate or estimate for now as; it may be related to glucose level or something else and these changing may possibly affect the elasticity or viscosity of the cornea.

CONCLUSION

The mean CH and CRF values were found less in the diabetic group. A statistically significant difference was found between the diabetic and nondiabetic groups in terms of IOP parameters. Mean IOPcc and IOPg values were found high in the diabetic group. We believe that this will provide a base that will shed light on other work needs to be done.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This prospective case-control study was approved by the Faculty of Medicine, Adnan Menderes University, Ethics Committee for Non-Interventional Clinical Investigations, Aydin, Turkey.

HUMAN AND ANIMAL RIGHTS

No Animals were used in this research. All human research procedures followed were in accordance with the ethical standards of the committee responsible for human experimentation (institutional and national), and with the Helsinki Declaration of 1975, as revised in 2013.

CONSENT FOR PUBLICATION

A written informed consent was obtained from all patients when they were enrolled.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Declared none.

REFERENCES

[1] Luce DA. Determining in vivo biomechanical properties of the cornea with an ocular response analyzer. J Cataract Refract Surg 2005; 31(1): 156-62.[http://dx.doi.org/10.1016/j.jcrs.2004.10.044] [PMID: 15721708]
[2] Kotecha A. What biomechanical properties of the cornea are relevant for the clinician? Surv Ophthalmol 2007; 52(Suppl. 2): S109-14.[http://dx.doi.org/10.1016/j.survophthal.2007.08.004] [PMID: 17998034]
[3] Chihara E. Assessment of true intraocular pressure: The gap between theory and practical data. Surv Ophthalmol 2008; 53(3): 203-18.[http://dx.doi.org/10.1016/j.survophthal.2008.02.005] [PMID: 18501267]
[4] Goebbels M. Tear secretion and tear film function in insulin dependent diabetics. Br J Ophthalmol 2000; 84(1): 19-21.[http://dx.doi.org/10.1136/bjo.84.1.19] [PMID: 10611093]
[5] Bron AM, Creuzot-Garcher C, Goudeau-Boutillon S, d’Athis P. Falsely elevated intraocular pressure due to increased central corneal thickness. Graefes Arch Clin Exp Ophthalmol 1999; 237(3): 220-4.[http://dx.doi.org/10.1007/s004170050222] [PMID: 10090585]
[6] Inoue K, Kato S, Inoue Y, Amano S, Oshika T. The corneal endothelium and thickness in type II diabetes mellitus. Jpn J Ophthalmol 2002; 46(1): 65-9.[http://dx.doi.org/10.1016/S0021-5155(01)00458-0] [PMID: 11853716]
[7] Ravalico G, Tognetto D, Palomba M, Calderini S, Vattovani O. Corneal endothelial function in diabetes: A fluorophotometric study. Ophthalmologica 1994; 208(4): 179-84.[http://dx.doi.org/10.1159/000310482] [PMID: 7970543]
[8] Brandt JD, Beiser JA, Kass MA, Gordon MO. Central corneal thickness in the Ocular Hypertension Treatment Study (OHTS). Ophthalmology 2001; 108(10): 1779-88.[http://dx.doi.org/10.1016/S0161-6420(01)00760-6] [PMID: 11581049]
[9] Nemesure B, Wu SY, Hennis A, Leske MC. Corneal thickness and intraocular pressure in the Barbados eye studies. Arch Ophthalmol 2003; 121(2): 240-4.[http://dx.doi.org/10.1001/archopht.121.2.240] [PMID: 12583791]
[10] Lee JS, Oum BS, Choi HY, Lee JE, Cho BM. Differences in corneal thickness and corneal endothelium related to duration in diabetes. Eye (Lond) 2006; 20(3): 315-8.[http://dx.doi.org/10.1038/sj.eye.6701868] [PMID: 15832184]
[11] Scheler A, Spoerl E, Boehm AG. Effect of diabetes mellitus on corneal biomechanics and measurement of intraocular pressure. Acta Ophthalmol 2012; 90(6): e447-51.[http://dx.doi.org/10.1111/j.1755-3768.2012.02437.x] [PMID: 22691299]
[12] Cankaya C, Gunduz E, Doganay S, Ulutas O. Corneal biomechanical characteristics, intraocular pressure and central corneal thickness in patients with type 2 diabetes mellitus. J Clin Med Res 2012; 4(6): 79-83.
[13] del Buey MA, Cristóbal JA, Ascaso FJ, Lavilla L, Lanchares E. Biomechanical properties of the cornea in Fuchs’ corneal dystrophy. Invest Ophthalmol Vis Sci 2009; 50(7): 3199-202.[http://dx.doi.org/10.1167/iovs.08-3312] [PMID: 19255149]
[14] Moreno-Montañés J, Maldonado MJ, García N, Mendiluce L, García-Gómez PJ, Seguí-Gómez M. Reproducibility and clinical relevance of the ocular response analyzer in nonoperated eyes: Corneal biomechanical and tonometric implications. Invest Ophthalmol Vis Sci 2008; 49(3): 968-74.[http://dx.doi.org/10.1167/iovs.07-0280] [PMID: 18326720]
[15] Bilen O, Akinici A, Ertan A. Corneal hysteresis and corneal resistance factor in diabetic patients with proliferative diabetic retinopathy: A controlled study XXVI Congress of ESCRS Berlin.2008.
[16] Hirneiss C, Neubauer AS, Yu A, Kampik A, Kernt M. Corneal biomechanics measured with the ocular response analyser in patients with unilateral open-angle glaucoma. Acta Ophthalmol 2011; 89(2): e189-92.[http://dx.doi.org/10.1111/j.1755-3768.2010.02093.x] [PMID: 21288308]
[17] Bonovas S, Peponis V, Filioussi K. Diabetes mellitus as a risk factor for primary open-angle glaucoma: A meta-analysis. Diabet Med 2004; 21(6): 609-14.[http://dx.doi.org/10.1111/j.1464-5491.2004.01173.x] [PMID: 15154948]
[18] Schultz RO, Matsuda M, Yee RW, Edelhauser HF, Schultz KJ. Corneal endothelial changes in type I and type II diabetes mellitus. Am J Ophthalmol 1984; 98(4): 401-10.[http://dx.doi.org/10.1016/0002-9394(84)90120-X] [PMID: 6486211]
[19] McNamara NA, Brand RJ, Polse KA, Bourne WM. Corneal function during normal and high serum glucose levels in diabetes. Invest Ophthalmol Vis Sci 1998; 39(1): 3-17.[PMID: 9430539]
[20] Sahin A, Bayer A, Ozge G, Mumcuoglu T. Corneal biomechanical changes in diabetes mellitus and their influence on intraocular pressure measurements 2009.[http://dx.doi.org/10.1167/iovs.08-2763]
[21] Hennis A, Wu SY, Nemesure B, Leske MC. Hypertension, diabetes, and longitudinal changes in intraocular pressure. Ophthalmology 2003; 110(5): 908-14.[http://dx.doi.org/10.1016/S0161-6420(03)00075-7] [PMID: 12750088]
[22] Dielemans I, de Jong PT, Stolk R, Vingerling JR, Grobbee DE, Hofman A. Primary open-angle glaucoma, intraocular pressure, and diabetes mellitus in the general elderly population. The Rotterdam Study. Ophthalmology 1996; 103(8): 1271-5.[http://dx.doi.org/10.1016/S0161-6420(96)30511-3] [PMID: 8764798]

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