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Hydration Dependent Viscoelastic Tensile Behavior of Cornea

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Abstract

The cornea is a protective transparent connective tissue covering the front of the eye. The standard uniaxial tensile experiments are among the most popular techniques for investigating biomechanical properties of the cornea. This experimental method characterizes the stress–strain response of corneal strips immersed in a bathing solution. In the present study, the important roles of corneal hydration on tensile viscoelastic properties were investigated. The thickness was used as a surrogate for hydration and uniaxial tensile experiments were performed on bovine corneal samples with four different average thickness (hydration), i.e., 1100 μm (4.87 mg water/mg dry tissue), 900 μm (4.13 mg water/mg dry tissue), 700 μm (3.20 mg water/mg dry tissue), and 500 μm (1.95 mg water/mg dry tissue). The samples were immersed in mineral oil in order to prevent their swelling during the experiments. A quasilinear viscoelastic (QLV) model was used to analyze the experimental measurements and determine viscoelastic material constants. It was observed that both maximum and equilibrium (relaxed) stresses were exponentially increased with decreasing tissue thickness (hydration). Furthermore, the QLV model successfully captured the corneal viscoelastic response with an average R 2 value greater than 0.99. Additional experiments were conducted in OBSS in order to confirm that these significant changes in viscoelastic properties were because of corneal hydration and not the bathing solution. The findings of this study suggest that extra care must be taken in interpreting the results of earlier uniaxial tensile testings and their correspondence to the corneal biomechanical properties.

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References

  1. Abramowitch, S. D., and S. L. Woo. An improved method to analyze the stress relaxation of ligaments following a finite ramp time based on the quasi-linear viscoelastic theory. J. Biomech. Eng. 126:92–97, 2004.

    Article  PubMed  Google Scholar 

  2. Abramowitch, S. D., S. L. Woo, T. D. Clineff, and R. E. Debski. An evaluation of the quasi-linear viscoelastic properties of the healing medial collateral ligament in a goat model. Ann. Biomed. Eng. 32:329–335, 2004.

    Article  PubMed  Google Scholar 

  3. Anderson, K., A. El-Sheikh, and T. Newson. Application of structural analysis to the mechanical behaviour of the cornea. J. R. Soc. Lond. Interface 1:3–15, 2004.

    Article  CAS  Google Scholar 

  4. Boschetti, F., V. Triacca, L. Spinelli, and A. Pandolfi. Mechanical characterization of porcine corneas. J. Biomech. Eng. 134:031003–031009, 2012.

    Article  CAS  PubMed  Google Scholar 

  5. Boyce, B. L., J. M. Grazier, R. E. Jones, and T. D. Nguyen. Full-field deformation of bovine cornea under constrained inflation conditions. Biomaterials 29:3896–3904, 2008.

    Article  CAS  PubMed  Google Scholar 

  6. Boyce, B. L., R. E. Jones, T. D. Nguyen, and J. M. Grazier. Stress-controlled viscoelastic tensile response of bovine cornea. J. Biomech. 40:2367–2376, 2007.

    Article  CAS  PubMed  Google Scholar 

  7. Carew, E. O., A. Garg, J. E. Barber, and I. Vesely. Stress relaxation preconditioning of porcine aortic valves. Ann. Biomed. Eng. 32:563–572, 2004.

    Article  PubMed  Google Scholar 

  8. Cheng, X., H. Hatami-Marbini, and P. M. Pinsky. Modeling collagen-proteoglycan structural interactions in the human cornea. In: Computer Models in Biomechanics, edited by G. A. Holzapfel, and E. Kuhl. Heidelberg: Springer, 2013, pp. 11–24.

    Chapter  Google Scholar 

  9. Doehring, T. C., E. O. Carew, and I. Vesely. The effect of strain rate on the viscoelastic response of aortic valve tissue: a direct-fit approach. Ann. Biomed. Eng. 32:223–232, 2004.

    Article  PubMed  Google Scholar 

  10. Elsheikh, A., and D. Alhasso. Mechanical anisotropy of porcine cornea and correlation with stromal microstructure. Exp. Eye Res. 88:1084–1091, 2009.

    Article  CAS  PubMed  Google Scholar 

  11. Elsheikh, A., D. Alhasso, and P. Rama. Biomechanical properties of human and porcine corneas. Exp. Eye Res. 86:783–790, 2008.

    Article  CAS  PubMed  Google Scholar 

  12. Elsheikh, A., and K. Anderson. Comparative study of corneal strip extensometry and inflation tests. Journal of The Royal Society Interface 2:177–185, 2005.

    Article  PubMed Central  Google Scholar 

  13. Elsheikh, A., M. Brown, D. Alhasso, P. Rama, M. Campanelli, and D. Garway-Heath. Experimental assessment of corneal anisotropy. J. Refract. Surg. 24:178–187, 2008.

    PubMed  Google Scholar 

  14. Elsheikh, A., W. Kassem, and S. W. Jones. Strain-rate sensitivity of porcine and ovine corneas. Acta Bioeng. Biomech. 13:25–36, 2011.

    PubMed  Google Scholar 

  15. Elsheikh, A., D. Wang, and D. Pye. Determination of the modulus of elasticity of the human cornea. J. Refract. Surg. 23:808–818, 2007.

    PubMed  Google Scholar 

  16. Fricke, T. R., B. A. Holden, D. A. Wilson, et al. Global cost of correcting vision impairment from uncorrected refractive error. Bull. World Health Organ. 90:728–738, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Fung, Y. C. Biomechanics: Mechanical Properties of Living Tissues (2nd ed.). New York: Springer, 1993.

    Book  Google Scholar 

  18. Han, L., D. Dean, L. A. Daher, A. J. Grodzinsky, and C. Ortiz. Cartilage aggrecan can undergo self-adhesion. Biophys. J. 95:4862–4870, 2008.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Hatami-Marbini, H., and E. Etebu. An experimental and theoretical analysis of unconfined compression of corneal stroma. J. Biomech. 46:1752–1758, 2013.

    Article  PubMed  Google Scholar 

  20. Hatami-Marbini, H., and E. Etebu. Hydration dependent biomechanical properties of the corneal stroma. Exp. Eye Res. 116:47–54, 2013.

    Article  CAS  PubMed  Google Scholar 

  21. Hatami-Marbini, H., and E. Etebu. A New Method to Determine Rate-dependent Material Parameters of Corneal Extracellular Matrix. Ann. Biomed. Eng. 41:2399–2408, 2013.

    Article  PubMed  Google Scholar 

  22. Hatami-Marbini, H., E. Etebu, and A. Rahimi. Swelling Pressure and Hydration Behavior of Porcine Corneal Stroma. Curr. Eye Res. 38:1124–1132, 2013.

    Article  CAS  PubMed  Google Scholar 

  23. Hatami-Marbini, H., and P. M. Pinsky. On mechanics of connective tissue: assessing the electrostatic contribution to corneal stroma elasticity. In: Material Research Society Proceedings, Boston, 2009, p. 1239.

  24. Hatami-Marbini, H., and A. Rahimi. Effects of bathing solution on tensile properties of the cornea. Exp. Eye Res. 120:103–108, 2014.

    Article  CAS  PubMed  Google Scholar 

  25. Hedbys, B. O., and C. H. Dohlman. A new method for the determination of the swelling pressure of the corneal stroma in vitro. Exp. Eye Res. 2:122–129, 1963.

    Article  CAS  PubMed  Google Scholar 

  26. Hedbys, B. O., and S. Mishima. The thickness-hydration relationship of the cornea. Exp. Eye Res. 5:221–228, 1966.

    Article  CAS  PubMed  Google Scholar 

  27. Hodson, S. Why the cornea Swells. J. Theor. Biol. 33:419–427, 1971.

    Article  CAS  PubMed  Google Scholar 

  28. Hodson, S. A. Corneal stromal swelling. Prog. Retin. Eye Res. 16:99–116, 1997.

    Article  CAS  Google Scholar 

  29. Hoeltzel, D. A., P. Altman, K. Buzard, and K.-I. Choe. Strip Extensiometry for Comparison of the Mechanical Response of Bovine, Rabbit, and Human Corneas. J. Biomech. Eng. 114:202–215, 1992.

    Article  CAS  PubMed  Google Scholar 

  30. Howland, H. C., R. H. Rand, and S. R. Lubkin. A thin-shell model of the cornea and its application to corneal surgery. Refract. Corneal Surg. 8:183–186, 1992.

    CAS  PubMed  Google Scholar 

  31. Iatridis, J. C., L. A. Setton, M. Weidenbaum, and V. C. Mow. The viscoelastic behavior of the non-degenerate human lumbar nucleus pulposus in shear. J. Biomech. 30:1005–1013, 1997.

    Article  CAS  PubMed  Google Scholar 

  32. Jue, B., and D. M. Maurice. The mechanical properties of the rabbit and human cornea. J. Biomech. 19:847–853, 1986.

    Article  CAS  PubMed  Google Scholar 

  33. Kampmeier, J., B. Radt, R. Birngruber, and R. Brinkmann. Thermal and Biomechanical Parameters of Porcine Cornea. Cornea 19:355–363, 2000.

    Article  CAS  PubMed  Google Scholar 

  34. Kim, W., A. Argento, F. W. Rozsa, and K. Mallett. Constitutive behavior of ocular tissues over a range of strain rates. J. Biomech. Eng. 134:061002-061002, 2012.

    Google Scholar 

  35. Lari, D. R., D. S. Schultz, A. S. Wang, O. T. Lee, and J. M. Stewart. Scleral mechanics: comparing whole globe inflation and uniaxial testing. Exp. Eye Res. 94:128–135, 2012.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Lee, R. E., and P. F. Davison. The collagens of the developing bovine cornea. Exp. Eye Res. 39:639–652, 1984.

    Article  CAS  PubMed  Google Scholar 

  37. Lewis, P. N., C. Pinali, R. D. Young, K. M. Meek, A. J. Quantock, and C. Knupp. Structural Interactions between Collagen and Proteoglycans Are Elucidated by Three-Dimensional Electron Tomography of Bovine Cornea. Structure 18:239–245, 2010.

    Article  CAS  PubMed  Google Scholar 

  38. Maurice, D. M. The cornea and sclera. In: The Eye, edited by H. Davason. London: Academic Press, pp. 1–184, 1984.

  39. Meek, K. M. The cornea and sclera. In: Collagen: Structure and Mechanics, edited by P. Fratzl. New York: Springer, pp. 359–396, 2008.

  40. Meek, K. M., N. J. Fullwood, P. H. Cooke, et al. Synchrotron x-ray diffraction studies of the cornea, with implications for stromal hydration. Biophys. J. 60:467–474, 1991.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Nigul, I., and U. Nigul. On algorithms of evaluation of Fung’s relaxation function parameters. J Biomech 20:343–352, 1987.

    Article  CAS  PubMed  Google Scholar 

  42. Nyquist, G. W. Rheology of the cornea: experimental techniques and results. Exp. Eye Res. 7:183–188, 1968.

    Article  CAS  PubMed  Google Scholar 

  43. Olsen, T., and S. Sperling. The swelling pressure of the human corneal stroma as determined by a new method. Exp. Eye Res. 44:481–490, 1987.

    Article  CAS  PubMed  Google Scholar 

  44. Pandolfi, A. Computational biomechanics of the human cornea. In: Computational Modeling in Biomechanics, edited by S. De, F. GuilaK, and M. Mofrad. New York: Springer, pp. 435–466, 2010.

  45. Pandolfi, A., and G. A. Holzapfel. Three-dimensional modeling and computational analysis of the human cornea considering distributed collagen fibril orientations. J. Biomech. Eng. 130:061006-061001-061006-061012, 2008.

    Google Scholar 

  46. Provenzano, P. P., R. S. Lakes, D. T. Corr, and R. Vanderby, Jr. Application of nonlinear viscoelastic models to describe ligament behavior. Biomech Model Mechanobiol 1:45–57, 2002.

    Article  CAS  PubMed  Google Scholar 

  47. Scott, J. E. Proteoglycan: collagen interactions and corneal ultrastructure. Biochem. Soc. Trans 19:877–881, 1991.

    CAS  PubMed  Google Scholar 

  48. Scott, J. E. Morphometry of cupromeronic blue-stained proteoglycan molecules in animal corneas, versus that of purified proteoglycans stained in vitro, implies that tertiary structures contribute to corneal ultrastructure. J. Anat. 180:155–164, 1992.

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Scott, J. E., and T. R. Bosworth. A comparative biochemical and ultrastructural study of proteoglycan-collagen interactions in corneal stroma - functional and metabolic implications. Biochem. J. 270:491–497, 1990.

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Smith, T. S. T., K. D. Frick, B. A. Holden, T. R. Fricke, and K. S. Naidoo. Potential lost productivity resulting from the global burden of uncorrected refractive errors. Bull. World Health Organ. 87:431–437, 2009.

    Google Scholar 

  51. Sverdlik, A., and Y. Lanir. Time-dependent mechanical behavior of sheep digital tendons, including the effects of preconditioning. Journal of Biomechanical Engineering-Transactions of the Asme 124:78–84, 2002.

    Article  CAS  Google Scholar 

  52. Wollensak, G., E. Spoerl, and T. Seiler. Stress-strain measurements of human and porcine corneas after riboflavin–ultraviolet-A-induced cross-linking. J. Cataract Refract. Surg. 29:1780–1785, 2003.

    Article  PubMed  Google Scholar 

  53. Woo, S. L., M. A. Gomez, and W. H. Akeson. The time and history-dependent viscoelastic properties of the canine medical collateral ligament. J. Biomech. Eng. 103:293–298, 1981.

    Article  CAS  PubMed  Google Scholar 

  54. Woo, S. L., A. S. Kobayashi, W. A. Schlegel, and C. Lawrence. Nonlinear material properties of intact cornea and sclera. Exp. Eye Res. 14:29–39, 1972.

    Article  CAS  PubMed  Google Scholar 

  55. Zeng, Y., J. Yang, K. Huang, Z. Lee, and X. Lee. A comparison of biomechanical properties between human and porcine cornea. J. Biomech. 34:533–537, 2001.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This project has been funded in whole or in part with the start-up fund from Oklahoma State University. The author would like to thank the members of computational biomechanics laboratory.

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  1. School of Mechanical and Aerospace Engineering, Oklahoma State University, 218 Engineering North, Stillwater, OK, 74078-5016, USA

    Hamed Hatami-Marbini

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Correspondence to Hamed Hatami-Marbini.

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Associate Editor Dan Elson oversaw the review of this article.

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Hatami-Marbini, H. Hydration Dependent Viscoelastic Tensile Behavior of Cornea. Ann Biomed Eng 42, 1740–1748 (2014). https://doi.org/10.1007/s10439-014-0996-6

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