Anisotropy and viscoelasticity of different corneal regions in rabbit corneal ectasia model_Journal of Biomedical Engineering

Authors：

WEI Junchao ¹ , CHEN Peng ² , HAN Pengfei ² , LIU Xiaona ¹ , HOU Jie ¹ , WU Ce ¹ , SONG Jie ¹ ,  CHEN Weiyi ¹ ,  LI Xiaona ¹

1. College of Biomedical Engineering, Taiyuan University of Technology, Taiyuan 030024, P. R. China;
2. Shanxi Aier Eye Hospital, Taiyuan 030012, P. R. China;

Corresponding author：

CHEN Weiyi, Email: chenweiyi@tyut.edu.cn; LI Xiaona, Email: lixiaona@tyut.edu.cn

Keywords：

Corneal ectasia; Anisotropy; Viscoelasticity; Creep

DOI：

10.7507/1001-5515.202312022

Video：

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The mechanical properties of the cornea in corneal ectasia disease undergo a significant reduction, yet the alterations in mechanical properties within distinct corneal regions remain unclear. In this study, we established a rabbit corneal ectasia model by employing collagenase II to degrade the corneal matrix within a central diameter of 6 mm. Optical coherence tomography was employed for the in vivo assessment of corneal morphology (corneal thickness and corneal curvature) one month after operation. Anisotropy and viscoelastic characteristics of corneal tissue were evaluated through biaxial and uniaxial testing, respectively. The results demonstrated a marked decrease in central corneal thickness, with no significant changes observed in corneal curvature. Under different strains, the elastic modulus of the cornea exhibited no significant differences in the up-down and naso-temporal directions between the control and model groups. However, the cornea in the model group displayed a significantly lower elastic modulus compared to the control group. Specifically, the elastic modulus of the central region cornea in the model group was significantly lower than that of the entire cornea within the same group. Moreover, in comparison to the control group, the cornea in the model group exhibited a significant increase in both creep rate and overall deformation rate. The instantaneous modulus and equilibrium modulus were significantly reduced in the model cornea. No significant differences were observed between the entire cornea and the central cornea concerning these parameters. The results indicate that corneal anisotropy remains unchanged in collagenase-induced ectatic cornea. However, a significant reduction in viscoelastic properties is noticed. This study provides valuable insights for investigating changes in corneal mechanical properties within different regions of ectatic corneal disease.

Citation： WEI Junchao, CHEN Peng, HAN Pengfei, LIU Xiaona, HOU Jie, WU Ce, SONG Jie, CHEN Weiyi, LI Xiaona. Anisotropy and viscoelasticity of different corneal regions in rabbit corneal ectasia model. Journal of Biomedical Engineering, 2024, 41(1): 129-135, 143. doi: 10.7507/1001-5515.202312022 Copy

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2.	Kling S, Hafezi F. Corneal biomechanics-a review. Ophthalmic Physiol Opt, 2017, 37(3): 240-252..
3.	Xue C, Xiang Y, Shen M, et al. Preliminary investigation of the mechanical anisotropy of the normal human corneal stroma. J Ophthalmol, 2018, 2018: 1-7..
4.	Roberts C J, Dupps W J. Biomechanics of corneal ectasia and biomechanical treatments. J Cataract Refract Surg, 2014, 40(6): 991-998..
5.	Kerautret J, Colin J, Touboul D, et al. Biomechanical characteristics of the ectatic cornea. J Cataract Refract Surg, 2008, 34(3): 510-513..
6.	Mikula E, Winkler M, Juhasz T, et al. Axial mechanical and structural characterization of keratoconus corneas. Exp Eye Res, 2018, 175: 14-19..
7.	Ambekar R, Toussaint Jr. K C, Wagoner Johnson A. The effect of keratoconus on the structural, mechanical, and optical properties of the cornea. J Mech Behav Biomed Mater, 2011, 4(3): 223-236..
8.	Qian X, Ma T, Shih C-C, et al. Ultrasonic microelastography to assess biomechanical properties of the cornea. IEEE Trans Biomed Eng, 2019, 66(3): 647-655..
9.	Mikula E R, Jester J V, Juhasz T. Measurement of an elasticity map in the human cornea. Investig Ophthalmol Vis Sci, 2016, 57(7): 3282..
10.	赵科超, 王晓君, 陈维毅, 等. 正常角膜与圆锥角膜粘弹性的对比研究. 生物医学工程学杂志, 2019, 36(4): 613-618..
11.	Edmund C. Corneal elasticity and ocular rigidity in normal and keratoconic eyes. Acta Ophthalmol, 1988, 66(2): 134-140..
12.	Moghadam F A, Jahromy M H, Fazelipour S, et al. Induction of experimental keratoconus in mice using collagenase. Physiol Pharmacol, 13(2): 209-215..
13.	Qiao J, Li H, Tang Y, et al. A rabbit model of corneal ectasia generated by treatment with collagenase type II. BMC Ophthalmol, 2018, 18(1): 94..
14.	Hu Y, Huang Y, Chen Y, et al. Study on patterned photodynamic cross-linking for keratoconus. Exp Eye Res, 2021, 204: 108450..
15.	Wei J, He R, Wang X, et al. The corneal ectasia model of rabbit: a validity and stability study. Bioengineering, 2023, 10(4): 479..
16.	乔静, 李海丽, 宋文静, 等. Ⅱ型胶原酶构建兔角膜离体扩张模型. 中华眼视光学与视觉科学杂志, 2016, 18(5): 275-279..
17.	乔静, 李海丽, 宋文静, 等. Ⅱ型胶原酶构建在体角膜扩张动物模型的可行性研究. 中华实验眼科杂志, 2017, 35(11): 984-989..
18.	陈昕妍, 秦晓, 张海霞, 等. Ⅱ型胶原酶对兔角膜生物力学特性的影响. 中国组织工程研究, 2019, 23(22): 3556-3561..
19.	Flockerzi E, Häfner L, Xanthopoulou K, et al. Reliability analysis of successive corneal Visualization Scheimpflug technology measurements in different keratoconus stages. Acta Ophthalmol, 2022, 100(1): e83-e90..
20.	Yang K, Xu L, Fan Q, et al. Evaluation of new Corvis ST parameters in normal, post-LASIK, post-LASIK keratectasia and keratoconus eyes. Sci Rep, 2020, 10(1): 5676..
21.	Heidari Z, Hashemi H, Mohammadpour M, et al. Evaluation of corneal topographic, tomographic and biomechanical indices for detecting clinical and subclinical keratoconus: a comprehensive three-device study. Int J Ophthalmol, 2021, 14(2): 228-239..
22.	Zhang H, Tian L, Guo L, et al. Comprehensive evaluation of corneas from normal, forme fruste keratoconus and clinical keratoconus patients using morphological and biomechanical properties. Int Ophthalmol, 2021, 41(4): 1247-1259..
23.	Zhou D, Abass A, Eliasy A, et al. Microstructure-based numerical simulation of the mechanical behaviour of ocular tissue. J R Soc Interface, 2019, 16(154): 20180685..
24.	Zhang H, Eliasy A, Lopes B, et al. Stress-strain index map: a new way to represent corneal material stiffness. Front Bioeng Biotechnol, 2021, 9: 640434..
25.	Lopes B T, Padmanabhan P, Eliasy A, et al. In vivo assessment of localised corneal biomechanical deterioration with keratoconus progression. Front Bioeng Biotechnol, 2022, 10: 812507..
26.	Ruberti J W, Sinha Roy A, Roberts C J. Corneal biomechanics and biomaterials. Annu Rev Biomed Eng, 2011, 13(1): 269-295..
27.	Dias J M, Ziebarth N M. Anterior and posterior corneal stroma elasticity assessed using nanoindentation. Exp Eye Res, 2013, 115: 41-46..
28.	Spiru B, Kling S, Hafezi F, et al. Biomechanical properties of human cornea tested by two-dimensional extensiometry ex vivo in fellow eyes: femtosecond laser-assisted LASIK versus SMILE. J Refract Surg, 2018, 34(6): 419-423..
29.	Kamiya K, Shimizu K, Ohmoto F. Comparison of the changes in corneal biomechanical properties after photorefractive keratectomy and laser in situ keratomileusis. Cornea, 2009, 28(7): 765-769..
30.	Ortiz D, Piñero D, Shabayek M H, et al. Corneal biomechanical properties in normal, post-laser in situ keratomileusis, and keratoconic eyes. J Cataract Refract Surg, 2007, 33(8): 1371-1375..
31.	Scarcelli G, Besner S, Pineda R, et al. Biomechanical characterization of keratoconus corneas ex vivo with Brillouin microscopy. Investig Ophthalmol Vis Sci, 2014, 55(7): 4490..
32.	Besner S, Shao P, Scarcelli G, et al. Imaging of keratoconic and normal human cornea with a Brillouin imaging system// Ophthalmic Technologies XXVI. San Francisco: SPIE, 2016, 9693: 30..
33.	Meek K M, Boote C. The use of X-ray scattering techniques to quantify the orientation and distribution of collagen in the corneal stroma. Prog Retin Eye Res, 2009, 28(5): 369-392..
34.	Radner W, Zehetmayer M, Aufreiter R, et al. Interlacing and cross-angle distribution of collagen lamellae in the human cornea. Cornea, 1998, 17(5): 537-543..
35.	Elsheikh A, Alhasso D. Mechanical anisotropy of porcine cornea and correlation with stromal microstructure. Exp Eye Res, 2009, 88(6): 1084-1091..
36.	Arsalan Khan M, Elsheikh A, Ahmad Khan I. Biomechanical behaviour-anisotropy of eye cornea through experimental strip tests// IOP Conference Series: Materials Science and Engineering. Bengaluru: IOP, 2018, 310(1): 012075..
37.	Xiang Y, Shen M, Xue C, et al. Tensile biomechanical properties and constitutive parameters of human corneal stroma extracted by SMILE procedure. J Mech Behav Biomed Mater, 2018, 85: 102-108..

1. Gatzioufas Z, Seitz B. Determination of corneal biomechanical properties in vivo: a review. Mater Sci Technol, 2015, 31(2): 188-196..
2. Kling S, Hafezi F. Corneal biomechanics-a review. Ophthalmic Physiol Opt, 2017, 37(3): 240-252..
3. Xue C, Xiang Y, Shen M, et al. Preliminary investigation of the mechanical anisotropy of the normal human corneal stroma. J Ophthalmol, 2018, 2018: 1-7..
4. Roberts C J, Dupps W J. Biomechanics of corneal ectasia and biomechanical treatments. J Cataract Refract Surg, 2014, 40(6): 991-998..
5. Kerautret J, Colin J, Touboul D, et al. Biomechanical characteristics of the ectatic cornea. J Cataract Refract Surg, 2008, 34(3): 510-513..
6. Mikula E, Winkler M, Juhasz T, et al. Axial mechanical and structural characterization of keratoconus corneas. Exp Eye Res, 2018, 175: 14-19..
7. Ambekar R, Toussaint Jr. K C, Wagoner Johnson A. The effect of keratoconus on the structural, mechanical, and optical properties of the cornea. J Mech Behav Biomed Mater, 2011, 4(3): 223-236..
8. Qian X, Ma T, Shih C-C, et al. Ultrasonic microelastography to assess biomechanical properties of the cornea. IEEE Trans Biomed Eng, 2019, 66(3): 647-655..
9. Mikula E R, Jester J V, Juhasz T. Measurement of an elasticity map in the human cornea. Investig Ophthalmol Vis Sci, 2016, 57(7): 3282..
10. 赵科超, 王晓君, 陈维毅, 等. 正常角膜与圆锥角膜粘弹性的对比研究. 生物医学工程学杂志, 2019, 36(4): 613-618..
11. Edmund C. Corneal elasticity and ocular rigidity in normal and keratoconic eyes. Acta Ophthalmol, 1988, 66(2): 134-140..
12. Moghadam F A, Jahromy M H, Fazelipour S, et al. Induction of experimental keratoconus in mice using collagenase. Physiol Pharmacol, 13(2): 209-215..
13. Qiao J, Li H, Tang Y, et al. A rabbit model of corneal ectasia generated by treatment with collagenase type II. BMC Ophthalmol, 2018, 18(1): 94..
14. Hu Y, Huang Y, Chen Y, et al. Study on patterned photodynamic cross-linking for keratoconus. Exp Eye Res, 2021, 204: 108450..
15. Wei J, He R, Wang X, et al. The corneal ectasia model of rabbit: a validity and stability study. Bioengineering, 2023, 10(4): 479..
16. 乔静, 李海丽, 宋文静, 等. Ⅱ型胶原酶构建兔角膜离体扩张模型. 中华眼视光学与视觉科学杂志, 2016, 18(5): 275-279..
17. 乔静, 李海丽, 宋文静, 等. Ⅱ型胶原酶构建在体角膜扩张动物模型的可行性研究. 中华实验眼科杂志, 2017, 35(11): 984-989..
18. 陈昕妍, 秦晓, 张海霞, 等. Ⅱ型胶原酶对兔角膜生物力学特性的影响. 中国组织工程研究, 2019, 23(22): 3556-3561..
19. Flockerzi E, Häfner L, Xanthopoulou K, et al. Reliability analysis of successive corneal Visualization Scheimpflug technology measurements in different keratoconus stages. Acta Ophthalmol, 2022, 100(1): e83-e90..
20. Yang K, Xu L, Fan Q, et al. Evaluation of new Corvis ST parameters in normal, post-LASIK, post-LASIK keratectasia and keratoconus eyes. Sci Rep, 2020, 10(1): 5676..
21. Heidari Z, Hashemi H, Mohammadpour M, et al. Evaluation of corneal topographic, tomographic and biomechanical indices for detecting clinical and subclinical keratoconus: a comprehensive three-device study. Int J Ophthalmol, 2021, 14(2): 228-239..
22. Zhang H, Tian L, Guo L, et al. Comprehensive evaluation of corneas from normal, forme fruste keratoconus and clinical keratoconus patients using morphological and biomechanical properties. Int Ophthalmol, 2021, 41(4): 1247-1259..
23. Zhou D, Abass A, Eliasy A, et al. Microstructure-based numerical simulation of the mechanical behaviour of ocular tissue. J R Soc Interface, 2019, 16(154): 20180685..
24. Zhang H, Eliasy A, Lopes B, et al. Stress-strain index map: a new way to represent corneal material stiffness. Front Bioeng Biotechnol, 2021, 9: 640434..
25. Lopes B T, Padmanabhan P, Eliasy A, et al. In vivo assessment of localised corneal biomechanical deterioration with keratoconus progression. Front Bioeng Biotechnol, 2022, 10: 812507..
26. Ruberti J W, Sinha Roy A, Roberts C J. Corneal biomechanics and biomaterials. Annu Rev Biomed Eng, 2011, 13(1): 269-295..
27. Dias J M, Ziebarth N M. Anterior and posterior corneal stroma elasticity assessed using nanoindentation. Exp Eye Res, 2013, 115: 41-46..
28. Spiru B, Kling S, Hafezi F, et al. Biomechanical properties of human cornea tested by two-dimensional extensiometry ex vivo in fellow eyes: femtosecond laser-assisted LASIK versus SMILE. J Refract Surg, 2018, 34(6): 419-423..
29. Kamiya K, Shimizu K, Ohmoto F. Comparison of the changes in corneal biomechanical properties after photorefractive keratectomy and laser in situ keratomileusis. Cornea, 2009, 28(7): 765-769..
30. Ortiz D, Piñero D, Shabayek M H, et al. Corneal biomechanical properties in normal, post-laser in situ keratomileusis, and keratoconic eyes. J Cataract Refract Surg, 2007, 33(8): 1371-1375..
31. Scarcelli G, Besner S, Pineda R, et al. Biomechanical characterization of keratoconus corneas ex vivo with Brillouin microscopy. Investig Ophthalmol Vis Sci, 2014, 55(7): 4490..
32. Besner S, Shao P, Scarcelli G, et al. Imaging of keratoconic and normal human cornea with a Brillouin imaging system// Ophthalmic Technologies XXVI. San Francisco: SPIE, 2016, 9693: 30..
33. Meek K M, Boote C. The use of X-ray scattering techniques to quantify the orientation and distribution of collagen in the corneal stroma. Prog Retin Eye Res, 2009, 28(5): 369-392..
34. Radner W, Zehetmayer M, Aufreiter R, et al. Interlacing and cross-angle distribution of collagen lamellae in the human cornea. Cornea, 1998, 17(5): 537-543..
35. Elsheikh A, Alhasso D. Mechanical anisotropy of porcine cornea and correlation with stromal microstructure. Exp Eye Res, 2009, 88(6): 1084-1091..
36. Arsalan Khan M, Elsheikh A, Ahmad Khan I. Biomechanical behaviour-anisotropy of eye cornea through experimental strip tests// IOP Conference Series: Materials Science and Engineering. Bengaluru: IOP, 2018, 310(1): 012075..
37. Xiang Y, Shen M, Xue C, et al. Tensile biomechanical properties and constitutive parameters of human corneal stroma extracted by SMILE procedure. J Mech Behav Biomed Mater, 2018, 85: 102-108..

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Anisotropy and viscoelasticity of different corneal regions in rabbit corneal ectasia model

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