The corneoscleral shell of the eye: potentials of assessing biomechanical parameters in normal and pathological conditions

The paper reviews modern methods of evaluating the biomechanical properties of the corneoscleral shell of the eye that can be used both in the studies of the pathogenesis of various ophthalmic pathologies and in clinical practice. The biomechanical parameters of the cornea and the sclera have been shown to be diagnostically significant in assessing the risk of complications and the effectiveness of keratorefractive interventions, in the diagnosis and the prognosis of keratoconus, progressive myopia, or glaucoma. In clinical practice, a special device, Ocular Response Analyzer (ORA), has been used on a large scale. The analyzer is used to assess two parameters that characterize viscoelastic properties of the cornea — corneal hysteresis (CH) and corneal resistance factor (CRF). Reduced levels of CH and CRF have been noted after eximer laser surgery, especially that administered to patients who demonstrate a regression in the refraction effect or suffer from keratoconus. This fact justifies the use of these biomechanical parameters as additional diagnostic criteria in the evaluation of the state of the cornea. At the same time, ORA data are shown to reflect the biomechanical response to the impact of the air pulse not only from the cornea alone but also from the whole corneoscleral capsule. This is probably the cause of reduced CH in children with progressive myopia and a weakened supportive function of the sclera, as well as such reduction in glaucomatous adult patients. It is hypothesized that a low CH value is a result of remodeling of the connective tissue matrix of the corneoscleral shell of the eye and can be an independent factor testifying to a risk of glaucoma progression. Reduced CH in primary open-angle glaucoma occurs in parallel with the development of pathological structural changes of the optic disc, and deterioration of visual fields, which is an evidence of a specific character and sensitivity of this parameter. The values were compared under compensated intraocular pressure. Further improvement of noncontact and noninvasive techniques of the assessment of the biomechanical status of the cornea and the sclera and their introduction into clinical practice will improve the diagnosis of various eye pathologies in any way related to disorders of the supporting functions of the corneoscleral shell.

1. Iomdina E. N., Bauer S. M., Kotlyar K. E. [Biomechanics of eyes: theoretical aspects and clinical applications] Biomekhanika glaza: teoreticheskie aspekty i klinicheskie prilozheniya. Moscow: Real’noe vremya; 2015. (in Russ.).

2. Eilaghi A., Flanagan J. G., Simmons C. A., Ethier C. R. Effects of scleral stiffness properties on optic nerve head biomechanics. Ann Biomed Eng 2010;38 (4):1586‑1592.

3. Sigal I. A., Flanagan J. G., Ethier C. R. Factors influencing optic nerve head biomechanics. Invest Ophthalmol Vis Sci 2005;46 (11):4189‑4199.

4. Sigal I. A., Flanagan J. G., Tertinegg I., Ethier C. R. Finite element modeling of optic nerve head biomechanics. Invest Ophthalmol Vis Sci 2004;45 (12):4378‑4387.

5. Аvetisov S. E., Bubnova I. A., Antonov A. A. [The study of the effect of the corneal biomechanical properties on the intraocular pressure measurement]. Issledovanie vliyaniya biomekhanicheskikh svoistv rogovitsy na pokazateli tonometrii [Sibirskii nauchnyi meditsinskii zhurnal]. The Siberian Scientific Medical Journal. 2009;29 (4):30‑33. (In Russ.).

6. Orssengo G. J., Pye D. C. Determination of the true intraocular pressure and modulus of elasticity of the human cornea in vivo. Bull Math Biol 1999;61 (3):551‑572.

7. Swarbrick H. A. Orthokeratology review and update. Clin Exp Optom 2006;89 (3):124‑143.

8. Uchio E., Ohno S., Kudoh J., Aoki K., Kisielewicz L. T. Simulation model of an eyeball based on finite element analysis on a supercomputer. Br J Ophthalmol 1999;83 (10):1106‑1111.

9. Alastrue V., Calvo B., Pena E., Doblare M. Biomechanical modeling of refractive corneal surgery. J Biomech Eng 2006;128 (1):150‑160.

10. Roberts C. Biomechanics of the cornea and wavefront-guided laser refractive surgery. J Refract Surg 2002;18 (5):S589–592.

11. Iomdina E. N. [Biomechanical and biochemical disturbances in the sclera of progressive myopia and methods of their correction] Biomekhanicheskie i biokhimicheskie narusheniya sklery pri progressiruyushchei blizorukosti i metody ikh korrektsii. In: Avetisov S. E., Kashchenko T. P., Shamshinova A. M. Visual functions and their correction in children. Moscow: Meditsina; 2006. p. 163‑183. (in Russ.).

12. Pinero D. P., Alio J. L., Barraquer R. I., Michael R., Jimenez R. Corneal biomechanics, refraction, and corneal aberrometry in keratoconus: an integrated study. Invest Ophthalmol Vis Sci 2010;51 (4):1948‑1955.

13. Quigley H. A. The contribution of the sclera and lamina cribrosa to the pathogenesis of glaucoma: Diagnostic and treatment implications. Prog Brain Res 2015;220:59‑86.

14. Eilaghi A., Flanagan J. G., Tertinegg I., Simmons C. A., Wayne Brodland G., Ross Ethier C. Biaxial mechanical testing of human sclera. J Biomech 2010;43 (9):1696‑1701.

15. Elsheikh A., Geraghty B., Alhasso D., Knappett J., Campanelli M., Rama P. Regional variation in the biomechanical properties of the human sclera. Exp Eye Res 2010;90 (5):624‑633.

16. Girard M. J., Downs J. C., Bottlang M., Burgoyne C. F., Suh J. K. Peripapillary and posterior scleral mechanics--part II: experimental and inverse finite element characterization. J Biomech Eng 2009;131 (5):051012.

17. Arciniegas A., Amaya L. E. Mechanical behavior of the sclera. Ophthalmologica 1986;193 (1-2):45‑55.

18. Friedenwald J. S. Contribution to the theory and practice of tonometry. American Journal of Ophthalmology 1937; (20):985‑1024.

19. Strakhov V. V., Alekseev V. V. [Dynamic rigidometriya] Dinamicheskaya rigidometriya. [Annals of Ophthalmology]. Vestnik oftal’mologii. 1995;1:18‑20. (in Russ.).

20. Pallikaris I. G., Kymionis G. D., Ginis H. S., Kounis G. A., Tsilimbaris M. K. Ocular rigidity in living human eyes. Invest Ophthalmol Vis Sci 2005;46 (2):409‑414.

21. Nesterov A. P., Bunin A. Ya., Katsnel’son L. A. [Intraocular pressure. Physiology and pathology] Vnutriglaznoe davlenie. Fiziologiya i patologiya. Moscow: Nauka; 1974. (in Russ.).

22. Brubaker R. F., Ezekiel S., Chin L., Young L., Johnson S. A., Beeler G. W. The stressstrain behavior of the corneoscleral envelope of the eye. I. Development of a system for making in vivo measurements using optical interferometry. Exp Eye Res 1975;21 (1):37‑46.

23. Brubaker R. F., Johnson S. A., Beeler G. W. The stress-strain behavior of the corneoscleral envelope of the eye. II. In vivo measurements in rhesus monkey eyes. Exp Eye Res 1977; 24 (5):425‑435.

24. Forster W., Kasprzak H., von Bally G., Busse H. [Qualitative analysis of the elasticity of the bovine cornea by holographic interferometry]. Klin Monbl Augenheilkd 1992;200 (1):54‑59.

25. Smolek M. Elasticity of the bovine sclera measured with real-time holographic interferometry. Am J Optom Physiol Opt 1988;65 (8):653‑660.

26. Nguyen T. M., Aubry J. F., Touboul D., Fink M., et al. Monitoring of cornea elastic properties changes during UV-A / riboflavin-induced corneal collagen cross-linking using supersonic shear wave imaging: a pilot study. Invest Ophthalmol Vis Sci 2012;53 (9):5948‑5954.

27. Scarcelli G., Besner S., Pineda R., Yun S. H. Biomechanical characterization of keratoconus corneas ex vivo with Brillouin microscopy. Invest Ophthalmol Vis Sci 2014;55 (7):4490‑4495.

28. Ho L. C., Sigal I. A., Jan N. J., Squires A., et al. Magic angle-enhanced MRI of fibrous microstructures in sclera and cornea with and without intraocular pressure loading. Invest Ophthalmol Vis Sci 2014;55 (9):5662‑5672.

29. Jayasuriya A. C., Ghosh S., Scheinbeim J. I., Lubkin V., Bennett G., Kramer P. A study of piezoelectric and mechanical anisotropies of the human cornea. Biosens Bioelectron 2003;18 (4):381‑387.

30. Anisimov S. I., Anisimova S. Yu., Smotrich E. A., Zavgorodnyaya T. S., Zolotorevskii K. A. [Keratotenzotopografy — new diagnostic possibilities for studying the biomechanical properties of the cornea] Keratotenzotopografiya — novye diagnosticheskie vozmozhnosti izucheniya biomekhanicheskikh svoistv rogovitsy. [Ophthalmology]. Oftal’mologiya. 2011;8 (4):13‑17. (in Russ.).

31. Kotecha A., Elsheikh A., Roberts C. R., Zhu H., Garway-Heath D. F. Corneal thickness-and age-related biomechanical properties of the cornea measured with the ocular response analyzer. Invest Ophthalmol Vis Sci 2006;47 (12):5337‑5347.

32. Luce D. A. Determining in vivo biomechanical properties of the cornea with an ocular response analyzer. J Cataract Refract Surg 2005;31 (1):156‑162.

33. Shah S., Laiquzzaman M., Cunliffe I., Mantry S. The use of the Reichert ocular response analyser to establish the relationship between ocular hysteresis, corneal resistance factor and central corneal thickness in normal eyes. Cont Lens Anterior Eye 2006;29 (5):257‑262.

34. Roy A. S., Shetty R., Kummelil M. K. Keratoconus: a biomechanical perspective on loss of corneal stiffness. Indian J Ophthalmol 2013;61 (8):392‑393.

35. Neroev V. V., Khandzhyan A. T., Manukyan I. V. [Assessment of influence of eksimerlazerny keratorefraktsionny operations of LASIK and FRK on biomechanical properties of a cornea] Otsenka vliyaniya eksimerlazernykh keratorefraktsionnykh operatsii ASIK i FRK na biomekhanicheskie svoistva rogovitsy. [Ophthalmology]. Oftal’mologiya. 2009;6 (1):24‑29. (in Russ.).

36. Uthoff D., Hebestedt K., Duncker G., Sickenberger H. [Multicentric study regarding assessment of the driving ability of LASIK and orthokeratology patients compared with conventionally corrected persons]. Klin Monbl Augenheilkd 2013;230 (3):255‑264.

37. de Medeiros F. W., Sinha-Roy A., Alves M. R., Wilson S. E., Dupps W. J., Jr. Differences in the early biomechanical effects of hyperopic and myopic laser in situ keratomileusis. J Cataract Refract Surg 2010;36 (6):947‑953.

38. Qazi M. A., Roberts C. J., Mahmoud A. M., Pepose J. S. Topographic and biomechanical differences between hyperopic and myopic laser in situ keratomileusis. J Cataract Refract Surg 2005;31 (1):48‑60.

39. Аvetisov S. E., Bubnova I. A., Antonov A. A. [Corneal biomechanics: clinical importance, evaluation, possibilities of sistemization of examination approaches]. Biomekhanicheskie svoistva rogovitsy: klinicheskoe znachenie, metody issledovaniya, vozmozhnosti sistematizatsii podkhodov k izucheniyu [Annals Ophthalmology]. Vestnik oftal’mologii 2010;126 (6):3‑7. (In Russ.).

40. Fontes B. M., Ambrosio Junior R., Jardim D., Velarde G. C., Nose W. Ability of corneal biomechanical metrics and anterior segment data in the differentiation of keratoconus and healthy corneas. Arq Bras Oftalmol 2010;73 (4):333‑337.

41. Shah S., Laiquzzaman M. Comparison of corneal biomechanics in pre and postrefractive surgery and keratoconic eyes by Ocular Response Analyser. Cont Lens Anterior Eye 2009;32 (3):129‑132.

42. Arutyunyan L. L. [Role of biomechanical properties of an eye in determination of target pressure] Rol’ biomekhanicheskikh svoistv glaza v opredelenii tselevogo davleniya. [Glaucoma]. Glaukoma 2007;6 (3):60‑67. (in Russ.).

43. Touboul D., Benard A., Mahmoud A. M., Gallois A., Colin J., Roberts C. J. Early biomechanical keratoconus pattern measured with an ocular response analyzer: curve analysis. J Cataract Refract Surg 2011;37 (12):2144‑2150.

44. Strakhov V. V., Alekseev V. V. [Influence of the central thickness of a cornea on the level of intraocular pressure in norm and at glaucoma] Vliyanie tsentral’noi tolshchiny rogovitsy na uroven’ vnutriglaznogo davleniya v norme i pri glaukome. [Glaucoma]. Glaukoma 2006;4:78‑83. (in Russ.).

45. Erichev V. P., Eremina M. V., Yakubova L. V., Aref’eva Yu.A. [The analyzer of biomechanical properties of an eye in an assessment viscous elasticheskikh properties of a cornea in healthy eyes] Analizator biomekhanicheskikh svoistv glaza v otsenke vyazko-elasticheskikh svoistv rogovitsy v zdorovykh glazakh. [Glaucoma]. Glaukoma 2007;1:11‑15. (in Russ.).

46. Fontes B. M., Ambrosio R., Jr., Salomao M., Velarde G. C., Nose W. Biomechanical and tomographic analysis of unilateral keratoconus. J Refract Surg 2010;26 (9):677‑681.

47. Schweitzer C., Roberts C. J., Mahmoud A. M., Colin J., Maurice-Tison S., Kerautret J. Screening of forme fruste keratoconus with the ocular response analyzer. Invest Ophthalmol Vis Sci 2010;51 (5):2403‑2410.

48. Iomdina E. N., Arutyunyan L. L., Katargina L. A. et al. [Interrelation of a kornealny hysteresis and structurally functional parameters of an optic nerve at different stages of primary open-angle glaucoma] Vzaimosvyaz’ korneal’nogo gisterezisa i strukturno-funktsional’nykh parametrov zritel’nogo nerva pri raznykh stadiyakh pervichnoi otkrytougol’noi glaukomy. [Annals of Ophthalmology]. Rossiiskii oftal’mologicheskii zhurnal 2009;2 (3):17‑23. (in Russ.).

49. Arutyunyan L. L., Erichev V. P., Filippova O. M., Akopyan A. I. [Vyazkoelastichesky properties of a cornea at primary open-angle glaucoma] Vyazkoelasticheskie svoistva rogovitsy pri pervichnoi otkrytougol’noi glaukome. [Glaucoma]. Glaukoma 2007;1:62‑65. (in Russ.).

50. Hommer A., Fuchsjager-Mayrl G., Resch H., Vass C., Garhofer G., Schmetterer L. Estimation of ocular rigidity based on measurement of pulse amplitude using pneumotonometry and fundus pulse using laser interferometry in glaucoma. Invest Ophthalmol Vis Sci 2008;49 (9):4046‑4050.

51. Schroeder B., Hager A., Kutschan A., Wiegand W. [Measurement of viscoelastic corneal parameters (corneal hysteresis) in patients with primary open angle glaucoma]. Ophthalmologe 2008;105 (10):916‑920.

52. Avetisov S. E., Novikov I. A., Bubnova I. A., Antonov A. A., Siplivyi V. I. Determination of corneal elasticity coefficient using the ORA database. Journal of Refractive Surgery 2010;26 (7):520‑524.

53. Аvetisov S. E., Petrov S. Yu., Bubnova I. A., Antonov A. A. Аvetisov К. S. [Impact of the central thickness of the cornea on the results of tonometry (a review of literature)]. Vliyanie tsentral’noi tolshchiny rogovitsy na rezul’taty tonometrii (obzor literatury) [Annals Ophthalmology]. Vestnik oftal’mologii 2008;124 (5):1‑7. (In Russ.).

54. Аvetisov S. E., Bubnova I. A., Antonov A. A. [Investigation of the biomechanical properties of the cornea in patients with normotensive and primary open-angle glaucoma]. Issledovanie biomekhanicheskikh svoistv rogovitsy u patsientov s normotenzivnoi i pervichnoi otkrytougol’noi glaukomoi [Annals Ophthalmology]. Vestnik oftal’mologii 2008;124 (5):14‑16. (In Russ.).

55. Ang G. S., Bochmann F., Townend J., Azuara-Blanco A. Corneal biomechanical properties in primary open angle glaucoma and normal tension glaucoma. J Glaucoma 2008;17 (4):259‑262.

56. Medeiros F. A., Weinreb R. N. Evaluation of the influence of corneal biomechanical properties on intraocular pressure measurements using the ocular response analyzer. J Glaucoma 2006;15 (5):364‑370.

57. Anand A., De Moraes C. G., Teng C. C., Tello C., Liebmann J. M., Ritch R. Corneal hysteresis and visual field asymmetry in open angle glaucoma. Invest Ophthalmol Vis Sci 2010;51 (12):6514‑6518.

58. Sun L., Shen M., Wang J., Fang A., et al. Recovery of corneal hysteresis after reduction of intraocular pressure in chronic primary angle-closure glaucoma. Am J Ophthalmol 2009;147 (6):1061‑1066,1066 e1061–1062.

59. Carbonaro F., Hysi P. G., Fahy S. J., Nag A., Hammond C. J. Optic disc planimetry, corneal hysteresis, central corneal thickness, and intraocular pressure as risk factors for glaucoma. Am J Ophthalmol 2014;157 (2):441‑446.

60. Hong J., Xu J., Wei A., Deng S. X., et al. A new tonometer--the Corvis ST tonometer: clinical comparison with noncontact and Goldmann applanation tonometers. Invest Ophthalmol Vis Sci 2013;54 (1):659‑665.

61. Huseynova T., Waring G. O.t., Roberts C., Krueger R. R., Tomita M. Corneal biomechanics as a function of intraocular pressure and pachymetry by dynamic infrared signal and Scheimpflug imaging analysis in normal eyes. Am J Ophthalmol 2014;157 (4):885‑893.

62. Li J., Wang S., Manapuram R. K., Singh M., et al. Dynamic optical coherence tomography measurements of elastic wave propagation in tissue-mimicking phantoms and mouse cornea in vivo. J Biomed Opt 2013;18 (12):121503.