Correlation of Corneoscleral Membrane Biomechanical Properties and Eye Morphometric Parameters in Patients with Primary Open-Angle Glaucoma

Purpose: to study a correlation between morphometric parameters of the eye and tonometry data, taking into account viscoelastic properties of the cornea in patients with primary open-angle glaucoma (POAG), as well as in practically healthy individuals using different methods of tonometry. Patients and Methods. Correlations between morphometric parameters of the eye and tonometry data were studied in view of viscoelastic properties of the cornea in 51 patients with POAG who were observed at the “Optimed” Laser Vision Recovery Center in Ufa (99 eyes) and in 31 practically healthy individuals (62 eyes). Various methods of tonometry were used: tonometry according to Maklakov, contactless tonometry, tonometry with the Ocular Response Analyzer (ORA, Reichert Inc., USA), as well as ultrasound echobiometry, pachymetry. Results. The CH and CRF parameters reflecting the biomechanical properties of the corneoscleral membrane of the eye were close in value to each other with a high degree of positive correlation in the control group (ρ = 0.783, p < 0.001), with an average correlation in the group with POAG (ρ = 0.545, p < 0.001). In eyes with POAG, a negative CH correlation of average degree with corneal-compensated IOP (ρ = -0.572, p < 0.001), a negative CRF correlation of moderate degree with IOP by the Maklakov method (ρ = -0.346, p < 0.001) and corneal-compensated IOP with dynamic bi-directional applanation tonometry (ρ = -0.327, p = 0.001), low correlation with IOP using contactless tonometry (ρ = 0.243, p < 0.015) were observed. In the group of patients with POAG, a positive average correlation was found between the central thickness of the cornea and CRF (ρ = 0.398, p < 0.001), and CH (ρ = 0.368, p < 0.001), low correlation with IOP using contactless tonometry (ρ = 0.266, p = 0.008). Conclusion. Correlations of biomechanical properties of the corneoscleral membrane and morphometric parameters of the eye in patients with POAG were revealed using different methods of tonometry. In the group of patients with POAG and in the control group, positive correlations of the central thickness of the cornea with the IOP level in tonometry were determined by the contactless method, as well as with the main ORA parameters reflecting the visco-elastic properties of the fibrous membrane of the eye — the corneal resistance factor, corneal hysteresis.

1. 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– 92. DOI: 10.1007/s10439-009-9879-7

2. Журавлева А.Н., Нероев В.В., Теплинская Л.Е., Андреева Л.Д. Изучение тканевого и плазменного фибронектина при первичной открытоугольной глаукоме. Офтальмология. 2009;(6)3:15–9. [Zhuravleva A.N., Neroev V.V., Tep linskaya L.E., Andreeva L.D. Study of tissue and plasma fibronectin in primary open-angle glaucoma. Ophthalmology in Russia = Oftal’mologiya. 2009;6(3):15–9 (In Russ.)].

3. Yaoeda K., Fukushima A., Shirakashi M., Fukuchi T. Comparison of intraocular pressure adjusted by central corneal thickness or corneal biomechanical properties as measured in glaucomatous eyes using noncontact tonometers and the Goldmann applanation tonometer. Clin Ophthalmol. 2016;10:829–34. DOI: 10.2147/OPTH. S106836

4. Hong Y., Shoji N., Morita T., Hirasawa K., Matsumura K., Kasahara M., Shimizu K. Comparison of corneal biomechanical properties in normal tension glaucoma patients with different visual field progression speed. International J Ophthalmol. 2016;9(7):973–8. DOI:10.18240/ijo.2016.07.06

5. Егоров Е.А., Васина М.В. Значение исследования биомеханических свойств роговой оболочки в оценке офтальмотонуса. РМЖ «Клиническая Офтальмология». 2008;1:1–3. [Egorov E.A., Vasina M.V. The value of the study of the biome chanical properties of the cornea in the assessment of the ophthalmotonus. Russian Medical Journal. Clinical Ophthalmology = Rossijskij medicinskij zhurnal. Klin icheskaya oftal’mologiya. 2008;1:1–3 (In Russ.)].

6. Страхов В.В., Алексеев В.В., Аль-Моррани А.М. Межокулярная асимметрия корнеального гистерезиса в норме и при первичной открытоугольной глау коме. Практическая медицина. 2012;59(4):244–7. [Strakhov V.V., Alekseev V.V., Al’-Morrani A.M. Interocular asymmetry of corneal hysteresis in norm and with primary open-angle glaucoma. Practical Medicine = Prakticheskaya meditsina. 2012;59(4):244–7 (In Russ.)].

7. Oncel B., Dinc U., Orge F., Yalvac B. Comparison of IOP measurement by ocular response analyzer, dynamic contour, Goldmann applanation, and non contact tonometry. Eur J Ophthalmol. 2009 Nov-Dec;19(6):936–41. DOI: 10.1177/112067210901900607

8. Jorge J., González-Méijome J.M., Queirós A., Fernandes P., Diaz-Rey J.A. A com parison of the NCT Reichert R7 with Goldmann applanation tonometry and the Reichert ocular response analyzer. Ophthalmic Physiol Opt. 2011;31(2):174–9. DOI: 10.1111/j.1475-1313.2010.00817.x

9. Kouchaki B., Hashemi H., Yekta A., Khabazkhoob M. Comparison of current to nometry techniques in measurement of intraocular pressure. Journal of Current Ophthalmology. 2017;29(2):92–7. DOI: 10.1016/j.joco.2016.08.010.J

10. Martinez-de-la-Casa J., Garcia-Feijoo J., Fernandez-Vidal A., Mendez-Hernan dez C., Garcia-Sanchez J. Ocular Response Analyzer versus Goldmann Applanation Tonometry for Intraocular Pressure Measurements. Investigative Ophthalmology & Visual Science October. 2006;47:4410–4. DOI: 10.1167/iovs.06-0158

11. De Moraes C.V., Hill V., Tello C., Liebmann J.M., Ritch R. Lower corneal hysteresis is associated with more rapid glaucomatous visual field progression. J Glaucoma. 2012;21(4):209–13. DOI: 10.1097/ijg.0b013e3182071b92

12. Medeiros F.A., Meira-Freitas D., Lisboa R., Kuang T.M., Zangwill L.M., Wein reb R.N. Corneal hysteresis as a risk factor for glaucoma progression: a prospec tive longitudinal study. Ophthalmology. 2013;120(8):1533–40. DOI: 10.1016/j.oph tha.2013.01.032

13. Jorge J., González-Méijome J.M., Queirós A., Fernandes P., Diaz-Rey J.A. A com parison of the NCT Reichert R7 with Goldmann applanation tonometry and the Reichert ocular response analyzer. Ophthalmic Physiol Opt. 2011;31(2):174–9. DOI: 10.1111/j.1475-1313.2010.00817.x

14. Волкова Н.В., Юрьева Т.Н., Грищук А.С., Михалевич И.М. Корреляции и по правочные коэффициенты при различных видах тонометрии. Биомеханика и биогеометрия фиброзной оболочки глаза. Сообщение 2. Национальный журнал глаукома. 2016;15(1):37–45. [Volkova N.V., Yur’eva T.N., Grishchuk A.S., Mikhalevich I.M. Correlations and correction factors for different types of tonom etry. Biomechanics and biogeometry of the fibrous membrane of the eye. Message 2. National Journal of Glaucoma = Natsional’nyi zhurnal glaukoma. 2016;15(1):37–45 (In Russ.)].

15. Lau W., Pye D. A clinical description of ocular response analyzer measurements. IOVS. 2011;52(6):2911–6. DOI: 10.1167/iovs.10-6763

16. Kamiya K., Shimizu K., Ohmoto F. Effect of aging on corneal biomechanical parameters using the ocular response analyzer. J Refract Surg. 2009;25:888–93. DOI: 10.3928/1081597x-20090917-10

17. 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):257–62. DOI: 10.1016/j.clae.2006.09.006

18. Lau W., Pye D. Changes in corneal biomechanics and applanation tonometry with induced corneal swelling. Invest Ophthalmol Vis Sci. 2011;16;52(6):3207–14. DOI: 10.1167/iovs.10-6754

19. Congdon N.G., Broman A.T., Bandeen-Roche K., Grover D., Quigley H.A. Central corneal thickness and corneal hysteresis associated with glaucoma damage. Am J Ophthalmol. 2006;141:868–75. DOI: 10.1016/j.ajo.2005.12.007

20. Detry-Morel M., Jamart J., Pourjavan S. Evaluation of corneal biomechanical properties with the reichert ocular response analyzer. Eur J Ophthalmol. 2010;21(2):138–48. DOI: 10.5301/ejo.2010.2150

21. Bayoumi N.H., Bessa A.S., El Massry A.A. Ocular response analyzer and goldmann applanation tonometry: a comparative study of findings. J Glaucoma. 2010;19(9):627–31. DOI: 10.1097/ijg.0b013e3181ca7e01

22. Pensyl D., Sullivan-Mee M., Torres-Monte M., Halverson K., Qualls C. Combining corneal hysteresis with central corneal thickness and intraocular pressure for glaucoma risk assessment. Eye (Lond). 2012;26(10):1349–1356. DOI: 10.1038/ eye.2012.164

23. Murphy M.L., Pokrovskaya O., Galligan M., O’Brien С. Corneal hysteresis in patients with glaucoma-like optic discs, ocular hypertension and glaucoma, BMC Ophhalmology. 2017;17:1. DOI: 10.1186/s12886-016-0396-9

24. Touboul D., Roberts C., Kerautret J., Garra C., Maurice-Tison S., Saubusse E., Colin J. Correlations between corneal hysteresis, intraocular pressure, and corneal central pachymetry. J Cataract Refract Surg. 2008;34(4):616–22. DOI: 10.1016/j. jcrs.2007.11.051

25. Deol M., Taylor D., Radcliffe N. Corneal hysteresis and its relevance to glaucoma. Curr Opin Ophthalmol. 2015;26(2):96–102. DOI: 10.1097/ICU.0000000000000130

26. Kamiya K., Shimizu K., Ohmoto F. Effect of aging on corneal biomechanical parameters using the ocular response analyzer. J Refract Surg. 2009;25:888–93. DOI: 10.3928/1081597x-20090917-10

27. Coudrillier B., Tian J., Alexander S., Myers K.M., Quigley H.A., Nguyen T.D. Biomechanics of the human posterior sclera: age-and glaucoma-related changes measured using inflation testing. Invest Ophthalmol Vis Sci. 2012;53:1714–28. DOI: 10.1167/iovs.11-8009

28. Cartwright N.E.K, Tyrer J.R., Marshall J. Age-related differences in the elasticity of the human cornea. Invest Ophthalmol Vis Sci. 2011;52:4324–9. DOI: 10.1167/ iovs.09-4798

29. Петров С.Ю., Рещикова В.С., Вострухин С.В., Агаджанян Т.М., Подгорная Н.Н. Исследование биомеханических свойств различных структур глаза: настоя щее и перспективы. Офтальмология. 2015;12(1):8–14. [Petrov S.Y., Reshchiko va V.S., Vostrukhin S.V., Agadzhanyan T.M., Podgornaya N.N. Ocular biomechanics study: current state and perspectives. Ophthalmology in Russia = Oftal’mologiya. 2015;12(1):8–14 (In Russ.)]. DOI: 10.18008/1816-5095-2015-1-8-14

30. Арутюнян Л.Л. Взаимоотношения структурно-функциональных параметров и уровня поперечной связанности коллагена склеры глаукомных глаз. Национальный журнал глаукома. 2015;14(4):5–12. [Arutunyan L.L. Relations between structural and functional parameters and levels of transverse collagen coupling of sclera of glaucoma eyes. National Journal of Glaucoma = Natsional’nyi zhurnal glaukoma. 2015;14(4):5–12 (In Russ.)].