Characterization of rabbit corneal biomechanical properties after corneal refractive surgery based on rapid loading-unloading uniaxial tensile test_Journal of Biomedical Engineering

Authors：

ZHANG Di ^1,2 , ZHANG Haixia ¹ ,  LI Lin ¹

1. School of Biomedical Engineering, Capital Medical University, Beijing Key Laboratory of Fundamental Research on Biomechanics in Clinical Application, Capital Medical University, Beijing 100069, P. R. China;
2. School of Radiology, Shandong First Medical University & Shandong Academy of Medical Sciences, Taian, Shandong 271016, P. R. China;

Corresponding author：

LI Lin, Email: lil@ccmu.edu.cn

Keywords：

Cornea; Corneal refractive surgery; Biomechanical properties; Uniaxial tensile test; Visco-hyperelasticity

DOI：

10.7507/1001-5515.202306041

Video：

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In order to understand how the biomechanical properties of rabbit cornea change over time after corneal ablation, 21 healthy adult rabbits were used in this study, with the left eye as experimental side and the right eye as the control side. Firstly, a lamellar knife was used to remove a portion of the anterior corneal surface tissue (30%~50% of the original corneal thickness) from the left eye of each rabbit, as an animal model simulating corneal refractive surgery. Secondly, postoperative experimental rabbits were kept for one, three, or six months until being euthanized. Strip specimens were produced using their corneas in vitro to perform a uniaxial tensile test with an average loading-unloading rate of approximately 0.16 mm/s. Finally, the visco-hyperelastic material constitutive model was used to fit the data. The results showed that there was a significant difference in the viscoelastic parameters of the corneas between the experimental and the control eyes at the first and third postoperative months. There was a difference in tangential modulus between the experimental and the control eyes at strain levels of 0.02 and 0.05 at the third postoperative month. There was no significant difference in biomechanical parameters between the experimental and the control eyes at the sixth postoperative month. These results indicate that compared with the control eyes, the biomechanical properties of the experimental eyes vary over postoperative time. At the third postoperative month, the ratio of corneal tangential modulus between the experimental and the control eyes significantly increased, and then decreased. This work lays a preliminary foundation for understanding the biomechanical properties of the cornea after corneal refractive surgery based on rapid testing data obtained clinically.

Citation： ZHANG Di, ZHANG Haixia, LI Lin. Characterization of rabbit corneal biomechanical properties after corneal refractive surgery based on rapid loading-unloading uniaxial tensile test. Journal of Biomedical Engineering, 2024, 41(1): 136-143. doi: 10.7507/1001-5515.202306041 Copy

1.	Qian Y, Chen X, Naidu R K, et al. Comparison of efficacy and visual outcomes after SMILE and FS-LASIK for the correction of high myopia with the sum of myopia and astigmatism from -10. 00 to -14.00 dioptres. Acta Ophthalmol, 2020, 98(2): e161-e172.
2.	Blum M, Lauer A S, Kunert K S, et al. 10-year results of small incision lenticule extraction. J Refract Surg, 2019, 35(10): 618-623.
3.	Moshirfar M, Tukan A N, Bundogji N, et al. Ectasia after corneal refractive surgery: a systematic review. Ophthalmol Ther, 2021, 10(4): 753-776.
4.	Asif M I, Bafna R K, Mehta J S, et al. Complications of small incision lenticule extraction. Indian J Ophthalmol, 2020, 68(12): 2711-2722.
5.	Wu Z, Wang Y, Zhang J, et al. Comparison of corneal biomechanics after microincision lenticule extraction and small incision lenticule extraction. Br J Ophthalmol, 2017, 101(5): 650-654.
6.	Cao K, Liu L, Yu T, et al. Changes in corneal biomechanics during small-incision lenticule extraction (SMILE) and femtosecond-assisted laser in situ keratomileusis (FS-LASIK). Lasers Med Sci, 2020, 35(3): 599-609.
7.	Fu D, Zhao Y, Zhou X. Corneal biomechanical properties after small incision lenticule extraction surgery on thin cornea. Curr Eye Res, 2021, 46(2): 168-173.
8.	Zhang J, Zheng L, Zhao X, et al. Corneal biomechanics after small-incision lenticule extraction versus Q-value-guided femtosecond laser-assisted in situ keratomileusis. J Curr Ophthalmol, 2016, 28(4): 181-187.
9.	Zhang H, Khan M A, Zhang D, et al. Corneal biomechanical properties after FS-LASIK with residual bed thickness less than 50% of the original corneal thickness. J Ophthalmol, 2018, 2018: 2752945.
10.	Wang X, Li X, Chen W, et al. Effects of ablation depth and repair time on the corneal elastic modulus after laser in situ keratomileusis. Biomed Eng Online, 2017, 16(1): 20.
11.	Kling S, Torres-Netto E A, Spiru B, et al. Quasi-static optical coherence elastography to characterize human corneal biomechanical properties. Invest Ophthalmol Vis Sci, 2020, 61(6): 29.
12.	Zhang D, Qin X, Zhang H, et al. Time-varying regularity of changes in biomechanical properties of the corneas after removal of anterior corneal tissue. Biomed Eng Online, 2021, 20(1): 113.
13.	张迪, 张海霞, 曾正, 等. 基于快、慢速加载单轴拉伸数据识别的角膜生物力学特性比较. 医用生物力学, 2022, 37(4): 669-675.
14.	Pandolfi A, Holzapfel G A. Three-dimensional modeling and computational analysis of the human cornea considering distributed collagen fibril orientations. J Biomech Eng, 2008, 130(6): 061006.
15.	Zhang H, Qian X, Li L, et al. Understanding the viscoelastic properties of rabbit cornea based on stress relaxation tests and cyclic uniaxial tests. J Mech Med Biol, 2017, 2017: 1740035.
16.	Liu T, Shen M, Li H, et al. Changes and quantitative characterization of hyper-viscoelastic biomechanical properties for young corneal stroma after standard corneal cross-linking treatment with different ultraviolet-A energies. Acta Biomater, 2020, 113: 438-451.
17.	Whitford C, Movchan N V, Studer H, et al. A viscoelastic anisotropic hyperelastic constitutive model of the human cornea. Biomech Model Mechanobiol, 2018, 17(1): 19-29.
18.	王辉, 乔媛慧, 刘志成. 利用应变能衰减率确定软组织单轴拉伸预调次数. 医用生物力学, 2013, 28(6): 602-605.
19.	Giri P, Azar D T. Risk profiles of ectasia after keratorefractive surgery. Curr Opin Ophthalmol, 2017, 28(4): 337-342.
20.	Formisano N, van der Putten C, Grant R, et al. Mechanical properties of bioengineered corneal stroma. Adv Healthc Mater, 2021, 10(20): e2100972.
21.	Blackburn B J, Jenkins M W, Rollins A M, et al. A review of structural and biomechanical changes in the cornea in aging, disease, and photochemical crosslinking. Front Bioeng Biotechnol, 2019, 7: 66.
22.	Yu M, Chen M, Dai J. Comparison of the posterior corneal elevation and biomechanics after SMILE and LASEK for myopia: a short- and long-term observation. Graefes Arch Clin Exp Ophthalmol, 2019, 257(3): 601-606.
23.	Hwang E S, Stagg B C, Swan R, et al. Corneal biomechanical properties after laser-assisted in situ keratomileusis and photorefractive keratectomy. Clin Ophthalmol, 2017, 11: 1785-1789.
24.	杨兴华, 王育良, 徐新荣, 等. 准分子激光屈光性角膜切削术后角膜厚度的变化. 临床眼科杂志, 1998, 6(1): 14-15, 69-70.
25.	Li H, Wang Y, Dou R, et al. Intraocular pressure changes and relationship with corneal biomechanics after SMILE and FS-LASIK. Invest Ophthalmol Vis Sci, 2016, 57(10): 4180-4186.
26.	Molladavoodi S, Robichaud M, Wulff D, et al. Corneal epithelial cells exposed to shear stress show altered cytoskeleton and migratory behaviour. PLoS One, 2017, 12(6): e0178981.
27.	Luft N, Ring M H, Dirisamer M, et al. Corneal epithelial remodeling induced by small incision lenticule extraction (SMILE). Invest Ophthalmol Vis Sci, 2016, 57(9): OCT176-OCT183.
28.	Romito N, Trinh L, Goemaere I, et al. Corneal remodeling after myopic SMILE: an optical coherence tomography and in vivo confocal microscopy study. J Refract Surg, 2020, 36(9): 597-605.
29.	Shetty R, Francis M, Shroff R, et al. Corneal biomechanical changes and tissue remodeling after SMILE and LASIK. Invest Ophthalmol Vis Sci, 2017, 58(13): 5703-5712.

1. Qian Y, Chen X, Naidu R K, et al. Comparison of efficacy and visual outcomes after SMILE and FS-LASIK for the correction of high myopia with the sum of myopia and astigmatism from -10. 00 to -14.00 dioptres. Acta Ophthalmol, 2020, 98(2): e161-e172.
2. Blum M, Lauer A S, Kunert K S, et al. 10-year results of small incision lenticule extraction. J Refract Surg, 2019, 35(10): 618-623.
3. Moshirfar M, Tukan A N, Bundogji N, et al. Ectasia after corneal refractive surgery: a systematic review. Ophthalmol Ther, 2021, 10(4): 753-776.
4. Asif M I, Bafna R K, Mehta J S, et al. Complications of small incision lenticule extraction. Indian J Ophthalmol, 2020, 68(12): 2711-2722.
5. Wu Z, Wang Y, Zhang J, et al. Comparison of corneal biomechanics after microincision lenticule extraction and small incision lenticule extraction. Br J Ophthalmol, 2017, 101(5): 650-654.
6. Cao K, Liu L, Yu T, et al. Changes in corneal biomechanics during small-incision lenticule extraction (SMILE) and femtosecond-assisted laser in situ keratomileusis (FS-LASIK). Lasers Med Sci, 2020, 35(3): 599-609.
7. Fu D, Zhao Y, Zhou X. Corneal biomechanical properties after small incision lenticule extraction surgery on thin cornea. Curr Eye Res, 2021, 46(2): 168-173.
8. Zhang J, Zheng L, Zhao X, et al. Corneal biomechanics after small-incision lenticule extraction versus Q-value-guided femtosecond laser-assisted in situ keratomileusis. J Curr Ophthalmol, 2016, 28(4): 181-187.
9. Zhang H, Khan M A, Zhang D, et al. Corneal biomechanical properties after FS-LASIK with residual bed thickness less than 50% of the original corneal thickness. J Ophthalmol, 2018, 2018: 2752945.
10. Wang X, Li X, Chen W, et al. Effects of ablation depth and repair time on the corneal elastic modulus after laser in situ keratomileusis. Biomed Eng Online, 2017, 16(1): 20.
11. Kling S, Torres-Netto E A, Spiru B, et al. Quasi-static optical coherence elastography to characterize human corneal biomechanical properties. Invest Ophthalmol Vis Sci, 2020, 61(6): 29.
12. Zhang D, Qin X, Zhang H, et al. Time-varying regularity of changes in biomechanical properties of the corneas after removal of anterior corneal tissue. Biomed Eng Online, 2021, 20(1): 113.
13. 张迪, 张海霞, 曾正, 等. 基于快、慢速加载单轴拉伸数据识别的角膜生物力学特性比较. 医用生物力学, 2022, 37(4): 669-675.
14. Pandolfi A, Holzapfel G A. Three-dimensional modeling and computational analysis of the human cornea considering distributed collagen fibril orientations. J Biomech Eng, 2008, 130(6): 061006.
15. Zhang H, Qian X, Li L, et al. Understanding the viscoelastic properties of rabbit cornea based on stress relaxation tests and cyclic uniaxial tests. J Mech Med Biol, 2017, 2017: 1740035.
16. Liu T, Shen M, Li H, et al. Changes and quantitative characterization of hyper-viscoelastic biomechanical properties for young corneal stroma after standard corneal cross-linking treatment with different ultraviolet-A energies. Acta Biomater, 2020, 113: 438-451.
17. Whitford C, Movchan N V, Studer H, et al. A viscoelastic anisotropic hyperelastic constitutive model of the human cornea. Biomech Model Mechanobiol, 2018, 17(1): 19-29.
18. 王辉, 乔媛慧, 刘志成. 利用应变能衰减率确定软组织单轴拉伸预调次数. 医用生物力学, 2013, 28(6): 602-605.
19. Giri P, Azar D T. Risk profiles of ectasia after keratorefractive surgery. Curr Opin Ophthalmol, 2017, 28(4): 337-342.
20. Formisano N, van der Putten C, Grant R, et al. Mechanical properties of bioengineered corneal stroma. Adv Healthc Mater, 2021, 10(20): e2100972.
21. Blackburn B J, Jenkins M W, Rollins A M, et al. A review of structural and biomechanical changes in the cornea in aging, disease, and photochemical crosslinking. Front Bioeng Biotechnol, 2019, 7: 66.
22. Yu M, Chen M, Dai J. Comparison of the posterior corneal elevation and biomechanics after SMILE and LASEK for myopia: a short- and long-term observation. Graefes Arch Clin Exp Ophthalmol, 2019, 257(3): 601-606.
23. Hwang E S, Stagg B C, Swan R, et al. Corneal biomechanical properties after laser-assisted in situ keratomileusis and photorefractive keratectomy. Clin Ophthalmol, 2017, 11: 1785-1789.
24. 杨兴华, 王育良, 徐新荣, 等. 准分子激光屈光性角膜切削术后角膜厚度的变化. 临床眼科杂志, 1998, 6(1): 14-15, 69-70.
25. Li H, Wang Y, Dou R, et al. Intraocular pressure changes and relationship with corneal biomechanics after SMILE and FS-LASIK. Invest Ophthalmol Vis Sci, 2016, 57(10): 4180-4186.
26. Molladavoodi S, Robichaud M, Wulff D, et al. Corneal epithelial cells exposed to shear stress show altered cytoskeleton and migratory behaviour. PLoS One, 2017, 12(6): e0178981.
27. Luft N, Ring M H, Dirisamer M, et al. Corneal epithelial remodeling induced by small incision lenticule extraction (SMILE). Invest Ophthalmol Vis Sci, 2016, 57(9): OCT176-OCT183.
28. Romito N, Trinh L, Goemaere I, et al. Corneal remodeling after myopic SMILE: an optical coherence tomography and in vivo confocal microscopy study. J Refract Surg, 2020, 36(9): 597-605.
29. Shetty R, Francis M, Shroff R, et al. Corneal biomechanical changes and tissue remodeling after SMILE and LASIK. Invest Ophthalmol Vis Sci, 2017, 58(13): 5703-5712.

Journal of Biomedical Engineering

Characterization of rabbit corneal biomechanical properties after corneal refractive surgery based on rapid loading-unloading uniaxial tensile test

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