Abstract
Aims
To determine the changes in corneal biomechanical parameters in patients with diabetes mellitus (DM) in comparison with controls.
Methods
Pertinent studies were identified by comprehensively search of PubMed, Embase, the Web of Science, the Cochrane Library, Scopus, the China National Knowledge Infrastructure and the Chinese biomedical disc (CBM) databases. Pooling analyses by random models using the D–L method were performed for corneal hysteresis (CH), the corneal resistance factor (CRF), corneal-compensated intraocular pressure (IOPcc) and Goldmann-correlated intraocular pressure (IOPg).
Results
A total of 15 studies were included in the final analysis, involving 1506 eyes in the diabetic group and 2190 eyes in the control group. The diabetic group had significantly higher CH, CRF, IOPg and IOPcc values than the control group. The pooled mean differences were 1.34 mmHg (95% confidence interval [CI] 0.60–2.08 mmHg, P < 0.001) for IOPg and 0.85 mmHg (95% CI 0.18–1.51 mmHg, P = 0.013) for IOPcc, 0.38 mmHg (95% CI 0.01–0.75, P = 0.047) for CH and 0.63 mmHg (95% CI 0.27–0.98, P = 0.001) for the CRF. Sensitivity analyses using the leave-one-out method showed a consistent significant difference between the groups (all P < 0.001).
Conclusions
Corneal biomechanics changed in the patients with DM. High CH, CRF, IOPcc and IOPg values may be associated factors for diabetes mellitus. Future studies are warranted to clarify the underlying mechanisms and explore the relationship between corneal biomechanics, glaucoma and diabetes mellitus.
Registration
PROSPERO registration No CRD4201705465.
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Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Zheng Y, Ley SH, Hu FB (2018) Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol 14:88–98
Ljubimov AV (2017) Diabetic complications in the cornea. Vis Res 139:138–152
Bikbova G, Oshitari T, Tawada A, Yamamoto S (2012) Corneal changes in diabetes mellitus. Curr Diabetes Rev 8:294–302
Wang W, Du S, Zhang X (2015) Corneal deformation response in patients with primary open-angle glaucoma and in healthy subjects analyzed by Corvis ST. Invest Ophthalmol Vis Sci 56:5557–5565
Luce DA (2005) Determining in vivo biomechanical properties of the cornea with an ocular response analyzer. J Cataract Refract Surg 31:156–162
Elsheikh A, Joda A, Abass A, Garway-Heath D (2015) Assessment of the ocular response analyzer as an instrument for measurement of intraocular pressure and corneal biomechanics. Curr Eye Res 40:1111–1119
Wang AS, Alencar LM, Weinreb RN et al (2013) Repeatability and reproducibility of Goldmann applanation, dynamic contour, and ocular response analyzer tonometry. J Glaucoma 22:127–132
David VP, Stead RE, Vernon SA (2013) Repeatability of ocular response analyzer metrics: a gender-based study. Optom Vis Sci 90:691–699
Kotecha A, White E, Schlottmann PG, Garway-Heath DF (2010) Intraocular pressure measurement precision with the Goldmann applanation, dynamic contour, and ocular response analyzer tonometers. Ophthalmology 117:730–737
Pinero DP, Alcon N (2015) Corneal biomechanics: a review. Clin Exp Optom 98:107–116
Chan MP, Grossi CM, Khawaja AP et al (2016) Associations with intraocular pressure in a large cohort: results from the UK biobank. Ophthalmology 123:771–782
Chua J, Nongpiur ME, Zhao W et al (2017) Comparison of corneal biomechanical properties between Indian and Chinese adults. Ophthalmology 124:1271–1279
Del BM, Casas P, Caramello C et al (2019) An update on corneal biomechanics and architecture in diabetes. J Ophthalmol 2019:7645352
Perez-Rico C, Gutierrez-Ortiz C, Gonzalez-Mesa A (2015) Effect of diabetes mellitus on Corvis ST measurement process. Acta Ophthalmol 93:e193–e198
Sahin A, Bayer A, Ozge G, Mumcuoglu T (2009) Corneal biomechanical changes in diabetes mellitus and their influence on intraocular pressure measurements. Invest Ophthalmol Vis Sci 50:4597–4604
Goldich Y, Barkana Y, Gerber Y et al (2009) Effect of diabetes mellitus on biomechanical parameters of the cornea. J Cataract Refract Surg 35:715–719
Ramm L, Herber R, Spoerl E, Pillunat LE, Terai N (2019) Measurement of corneal biomechanical properties in diabetes mellitus using the ocular response analyzer and the Corvis ST. Cornea 38:595–599
Schweitzer C, Korobelnik JF, Boniol M et al (2016) Associations of biomechanical properties of the cornea with environmental and metabolic factors in an elderly population: the ALIENOR study. Invest Ophthalmol Vis Sci 57:2003–2011
Yazgan S, Celik U, Kaldirim H et al (2014) Evaluation of the relationship between corneal biomechanic and HbA1C levels in type 2 diabetes patients. Clin Ophthalmol 8:1549–1553
Nalcacioglu-Yuksekkaya P, Sen E, Cetinkaya S, Bas V, Aycan Z, Ozturk F (2014) Corneal biomechanical characteristics in children with diabetes mellitus. Int Ophthalmol 34:881–886
Kara N, Yildirim Y, Univar T, Kontbay T (2013) Corneal biomechanical properties in children with diabetes mellitus. Eur J Ophthalmol 23:27–32
Scheler A, Spoerl E, Boehm AG (2012) Effect of diabetes mellitus on corneal biomechanics and measurement of intraocular pressure. Acta Ophthalmol 90:e447–e451
Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535
Wang W, Zhang X (2014) Choroidal thickness and primary open-angle glaucoma: a cross-sectional study and meta-analysis. Invest Ophthalmol Vis Sci 55:6007–6014
Beato JN, Esteves-Leandro J, Reis D et al (2019) Structural and biomechanical corneal differences between type 2 diabetic and nondiabetic patients. J Ophthalmol 2019:3764878
Bekmez S, Kocaturk T (2018) Higher intraocular pressure levels associated with lower hysteresis in type 2 diabetes. Open Ophthalmol J 12:29–33
Akkaya S, Can E, Ozturk F (2016) Comparison of the corneal biomechanical properties, optic nerve head topographic parameters, and retinal nerve fiber layer thickness measurements in diabetic and non-diabetic primary open-angle glaucoma. Int Ophthalmol 36:727–736
Narayanaswamy A, Chung RS, Wu RY et al (2011) Determinants of corneal biomechanical properties in an adult Chinese population. Ophthalmology 118:1253–1259
Kotecha A, Oddone F, Sinapis C et al (2010) Corneal biomechanical characteristics in patients with diabetes mellitus. J Cataract Refract Surg 36:1822–1828
Hager A, Wegscheider K, Wiegand W (2009) Changes of extracellular matrix of the cornea in diabetes mellitus. Graefes Arch Clin Exp Ophthalmol 247:1369–1374
Bao F, Deng M, Zheng X et al (2017) Effects of diabetes mellitus on biomechanical properties of the rabbit cornea. Exp Eye Res 161:82–88
Chen Y, Tsao SW, Heo M et al (2017) Age-stratified analysis of diabetes and pseudophakia effects on corneal endothelial cell density: a retrospective eye bank study. Cornea 36:367–371
Sanchis-Gimeno JA, Alonso L, Rahhal M, Bastir M, Perez-Bermejo M, Belda-Salmeron L (2017) Corneal thickness differences between type 2 diabetes and non-diabetes subjects during preoperative laser surgery examination. J Diabetes Complicat 31:209–212
Beckman RJ, Behndig A, Hallberg P, Linden C (2014) Increased corneal hysteresis after corneal collagen crosslinking: a study based on applanation resonance technology. JAMA Ophthalmol 132:1426–1432
Sudhahar V, Okur MN, Bagi Z et al (2018) Akt2 (protein kinase B beta) stabilizes ATP7A, a copper transporter for extracellular superoxide dismutase, in vascular smooth muscle: novel mechanism to limit endothelial dysfunction in type 2 diabetes mellitus. Arterioscler Thromb Vasc Biol 38:529–541
Zhao D, Cho J, Kim MH, Friedman DS, Guallar E (2015) Diabetes, fasting glucose, and the risk of glaucoma: a meta-analysis. Ophthalmology 122:72–78
Liu J, Roberts CJ (2005) Influence of corneal biomechanical properties on intraocular pressure measurement: quantitative analysis. J Cataract Refract Surg 31:146–155
Perez BF, Martinez DLCJ, Camacho BI et al (2018) Correlating corneal biomechanics and ocular biometric properties with lamina cribrosa measurements in healthy subjects. Semin Ophthalmol 33:223–230
Zhang B, Shweikh Y, Khawaja AP, Gallacher J, Bauermeister S, Foster PJ (2019) Associations with corneal hysteresis in a population cohort: results from 96 010 UK biobank participants. Ophthalmology 126:1500–1510
Akkaya S, Kucuk B, Dogan HK, Can E (2018) Evaluation of the lamina cribrosa in patients with diabetes mellitus using enhanced depth imaging spectral-domain optical coherence tomography. Diab Vasc Dis Res 15:442–448
Wu Z, Xu G, Weinreb RN, Yu M, Leung CK (2015) Optic nerve head deformation in glaucoma: a prospective analysis of optic nerve head surface and lamina cribrosa surface displacement. Ophthalmology 122:1317–1329
Khawaja AP, Rojas LK, Hardcastle AJ et al (2019) Genetic variants associated with corneal biomechanical properties and potentially conferring susceptibility to keratoconus in a genome-wide association study. JAMA Ophthalmol 137:1005–1012
Lanza M, Iaccarino S, Bifani M (2016) In vivo human corneal deformation analysis with a Scheimpflug camera, a critical review. J Biophoton 9:464–477
He M, Wang W, Ding H, Zhong X (2017) Corneal biomechanical properties in high myopia measured by dynamic scheimpflug imaging technology. Optom Vis Sci 94:1074–1080
Wang W, He M, He H, Zhang C, Jin H, Zhong X (2017) Corneal biomechanical metrics of healthy Chinese adults using Corvis ST. Contact Lens Anterior Eye 40:97–103
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GX, WW, MH and ZC conceived the idea and designed the study. XW, JW and LC collected the data. GX and WW performed the data analysis. All authors participated in the critical revision of the manuscript. All authors read and approved the final manuscript.
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This article belongs to the topical collection Eye Complications of Diabetes, managed by Giuseppe Querques.
Xiaoyi Wang, Guihua Xu and Wei Wang are Co-first authors.
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Wang, X., Xu, G., Wang, W. et al. Changes in corneal biomechanics in patients with diabetes mellitus: a systematic review and meta-analysis. Acta Diabetol 57, 973–981 (2020). https://doi.org/10.1007/s00592-020-01481-0
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DOI: https://doi.org/10.1007/s00592-020-01481-0