OSA's Digital Library

Biomedical Optics Express

Biomedical Optics Express

  • Editor: Joseph A. Izatt
  • Vol. 5, Iss. 5 — May. 1, 2014
  • pp: 1391–1402

Scleral birefringence as measured by polarization-sensitive optical coherence tomography and ocular biometric parameters of human eyes in vivo

Masahiro Yamanari, Satoko Nagase, Shinichi Fukuda, Kotaro Ishii, Ryosuke Tanaka, Takeshi Yasui, Tetsuro Oshika, Masahiro Miura, and Yoshiaki Yasuno  »View Author Affiliations


Biomedical Optics Express, Vol. 5, Issue 5, pp. 1391-1402 (2014)
http://dx.doi.org/10.1364/BOE.5.001391


View Full Text Article

Enhanced HTML    Acrobat PDF (6203 KB)





Browse Journals / Lookup Meetings

Browse by Journal and Year


   


Lookup Conference Papers

Close Browse Journals / Lookup Meetings

Article Tools

Share
Citations

Abstract

The relationship between scleral birefringence and biometric parameters of human eyes in vivo is investigated. Scleral birefringence near the limbus of 21 healthy human eyes was measured using polarization-sensitive optical coherence tomography. Spherical equivalent refractive error, axial eye length, and intraocular pressure (IOP) were measured in all subjects. IOP and scleral birefringence of human eyes in vivo was found to have statistically significant correlations (r = −0.63, P = 0.002). The slope of linear regression was −2.4 × 10−2 deg/μm/mmHg. Neither spherical equivalent refractive error nor axial eye length had significant correlations with scleral birefringence. To evaluate the direct influence of IOP to scleral birefringence, scleral birefringence of 16 ex vivo porcine eyes was measured under controlled IOP of 5−60 mmHg. In these ex vivo porcine eyes, the mean linear regression slope between controlled IOP and scleral birefringence was −9.9 × 10−4 deg/μm/mmHg. In addition, porcine scleral collagen fibers were observed with second-harmonic-generation (SHG) microscopy. SHG images of porcine sclera, measured on the external surface at the superior side to the cornea, showed highly aligned collagen fibers parallel to the limbus. In conclusion, scleral birefringence of healthy human eyes was correlated with IOP, indicating that the ultrastructure of scleral collagen was correlated with IOP. It remains to show whether scleral collagen ultrastructure of human eyes is affected by IOP as a long-term effect.

© 2014 Optical Society of America

OCIS Codes
(170.4470) Medical optics and biotechnology : Ophthalmology
(170.4500) Medical optics and biotechnology : Optical coherence tomography
(050.2555) Diffraction and gratings : Form birefringence
(180.4315) Microscopy : Nonlinear microscopy

ToC Category:
Ophthalmology Applications

History
Original Manuscript: January 13, 2014
Revised Manuscript: March 26, 2014
Manuscript Accepted: March 31, 2014
Published: April 3, 2014

Citation
Masahiro Yamanari, Satoko Nagase, Shinichi Fukuda, Kotaro Ishii, Ryosuke Tanaka, Takeshi Yasui, Tetsuro Oshika, Masahiro Miura, and Yoshiaki Yasuno, "Scleral birefringence as measured by polarization-sensitive optical coherence tomography and ocular biometric parameters of human eyes in vivo," Biomed. Opt. Express 5, 1391-1402 (2014)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-5-5-1391


Sort:  Author  |  Year  |  Journal  |  Reset  

References

  1. N. A. McBrien and A. Gentle, “Role of the sclera in the development and pathological complications of myopia,” Prog. Retin. Eye Res.22(3), 307–338 (2003). [CrossRef] [PubMed]
  2. C. F. Burgoyne, J. C. Downs, A. J. Bellezza, J. K. Suh, and R. T. Hart, “The optic nerve head as a biomechanical structure: a new paradigm for understanding the role of IOP-related stress and strain in the pathophysiology of glaucomatous optic nerve head damage,” Prog. Retin. Eye Res.24(1), 39–73 (2005). [CrossRef] [PubMed]
  3. J. A. Rada, S. Shelton, and T. T. Norton, “The sclera and myopia,” Exp. Eye Res.82(2), 185–200 (2006). [CrossRef] [PubMed]
  4. J. T. Siegwart and T. T. Norton, “Regulation of the mechanical properties of tree shrew sclera by the visual environment,” Vision Res.39(2), 387–407 (1999). [CrossRef] [PubMed]
  5. N. A. McBrien, L. M. Cornell, and A. Gentle, “Structural and ultrastructural changes to the sclera in a mammalian model of high myopia,” Invest. Ophthalmol. Vis. Sci.42(10), 2179–2187 (2001). [PubMed]
  6. J. K. Pijanka, B. Coudrillier, K. Ziegler, T. Sorensen, K. M. Meek, T. D. Nguyen, H. A. Quigley, and C. Boote, “Quantitative mapping of collagen fiber orientation in non-glaucoma and glaucoma posterior human sclerae,” Invest. Ophthalmol. Vis. Sci.53(9), 5258–5270 (2012). [CrossRef] [PubMed]
  7. J. C. Downs, J.-K. F. Suh, K. A. Thomas, A. J. Bellezza, R. T. Hart, and C. F. Burgoyne, “Viscoelastic material properties of the peripapillary sclera in normal and early-glaucoma monkey eyes,” Invest. Ophthalmol. Vis. Sci.46(2), 540–546 (2005). [CrossRef] [PubMed]
  8. B. Coudrillier, J. Tian, S. Alexander, K. M. Myers, H. A. Quigley, and T. D. Nguyen, “Biomechanics of the human posterior sclera: Age- and glaucoma-related changes measured using inflation testing,” Invest. Ophthalmol. Vis. Sci.53(4), 1714–1728 (2012). [CrossRef] [PubMed]
  9. A. J. Bellezza, C. J. Rintalan, H. W. Thompson, J. C. Downs, R. T. Hart, and C. F. Burgoyne, “Deformation of the lamina cribrosa and anterior scleral canal wall in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.44(2), 623–637 (2003). [CrossRef] [PubMed]
  10. H. Yang, H. Thompson, M. D. Roberts, I. A. Sigal, J. C. Downs, and C. F. Burgoyne, “Deformation of the early glaucomatous monkey optic nerve head connective tissue after acute IOP elevation in 3-D histomorphometric reconstructions,” Invest. Ophthalmol. Vis. Sci.52(1), 345–363 (2011). [CrossRef] [PubMed]
  11. H. A. Quigley, M. E. Dorman-Pease, and A. E. Brown, “Quantitative study of collagen and elastin of the optic nerve head and sclera in human and experimental monkey glaucoma,” Curr. Eye Res.10(9), 877–888 (1991). [CrossRef] [PubMed]
  12. S. Nagase, M. Yamanari, R. Tanaka, T. Yasui, M. Miura, T. Iwasaki, H. Goto, and Y. Yasuno, “Anisotropic alteration of scleral birefringence to uniaxial mechanical strain,” PLoS ONE8(3), e58716 (2013). [CrossRef] [PubMed]
  13. M. Yamanari, K. Ishii, S. Fukuda, Y. Lim, L. Duan, S. Makita, M. Miura, T. Oshika, and Y. Yasuno, “Optical rheology of porcine sclera by birefringence imaging,” PLoS ONE7(9), e44026 (2012). [CrossRef] [PubMed]
  14. R. Oldenbourg, E. D. Salmon, and P. T. Tran, “Birefringence of single and bundled microtubules,” Biophys. J.74(1), 645–654 (1998). [CrossRef] [PubMed]
  15. S. K. Nadkarni, M. C. Pierce, B. H. Park, J. F. de Boer, P. Whittaker, B. E. Bouma, J. E. Bressner, E. Halpern, S. L. Houser, and G. J. Tearney, “Measurement of collagen and smooth muscle cell content in atherosclerotic plaques using polarization-sensitive optical coherence tomography,” J. Am. Coll. Cardiol.49(13), 1474–1481 (2007). [CrossRef] [PubMed]
  16. C. J. Doillon, M. G. Dunn, E. Bender, and F. H. Silver, “Collagen fiber formation in repair tissue: development of strength and toughness,” Coll. Relat. Res.5(6), 481–492 (1985). [CrossRef] [PubMed]
  17. D. A. Parry, “The molecular and fibrillar structure of collagen and its relationship to the mechanical properties of connective tissue,” Biophys. Chem.29(1-2), 195–209 (1988). [CrossRef] [PubMed]
  18. G. D. Pins, D. L. Christiansen, R. Patel, and F. H. Silver, “Self-assembly of collagen fibers. influence of fibrillar alignment and decorin on mechanical properties,” Biophys. J.73(4), 2164–2172 (1997). [CrossRef] [PubMed]
  19. E. Götzinger, M. Pircher, M. Sticker, A. F. Fercher, and C. K. Hitzenberger, “Measurement and imaging of birefringent properties of the human cornea with phase-resolved, polarization-sensitive optical coherence tomography,” J. Biomed. Opt.9(1), 94–102 (2004). [CrossRef] [PubMed]
  20. Y. Yasuno, M. Yamanari, K. Kawana, M. Miura, S. Fukuda, S. Makita, S. Sakai, and T. Oshika, “Visibility of trabecular meshwork by standard and polarization-sensitive optical coherence tomography,” J. Biomed. Opt.15(6), 061705 (2010). [CrossRef] [PubMed]
  21. M. G. Ducros, J. D. Marsack, H. G. Rylander, S. L. Thomsen, and T. E. Milner, “Primate retina imaging with polarization-sensitive optical coherence tomography,” J. Opt. Soc. Am. A18(12), 2945–2956 (2001). [CrossRef]
  22. B. Cense, T. C. Chen, B. H. Park, M. C. Pierce, and J. F. de Boer, “Thickness and birefringence of healthy retinal nerve fiber layer tissue measured with polarization-sensitive optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.45(8), 2606–2612 (2004). [CrossRef] [PubMed]
  23. M. Yamanari, M. Miura, S. Makita, T. Yatagai, and Y. Yasuno, “Phase retardation measurement of retinal nerve fiber layer by polarization-sensitive spectral-domain optical coherence tomography and scanning laser polarimetry,” J. Biomed. Opt.13(1), 014013 (2008). [CrossRef] [PubMed]
  24. M. Miura, M. Yamanari, T. Iwasaki, A. E. Elsner, S. Makita, T. Yatagai, and Y. Yasuno, “Imaging polarimetry in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci.49(6), 2661–2667 (2008). [CrossRef] [PubMed]
  25. Y. Yasuno, M. Yamanari, K. Kawana, T. Oshika, and M. Miura, “Investigation of post-glaucoma-surgery structures by three-dimensional and polarization sensitive anterior eye segment optical coherence tomography,” Opt. Express17(5), 3980–3996 (2009). [CrossRef] [PubMed]
  26. Y. Lim, M. Yamanari, S. Fukuda, Y. Kaji, T. Kiuchi, M. Miura, T. Oshika, and Y. Yasuno, “Birefringence measurement of cornea and anterior segment by office-based polarization-sensitive optical coherence tomography,” Biomed. Opt. Express2(8), 2392–2402 (2011). [CrossRef] [PubMed]
  27. M. Yamanari, S. Makita, and Y. Yasuno, “Polarization-sensitive swept-source optical coherence tomography with continuous source polarization modulation,” Opt. Express16(8), 5892–5906 (2008). [CrossRef] [PubMed]
  28. M. Yamanari, Y. Lim, S. Makita, and Y. Yasuno, “Visualization of phase retardation of deep posterior eye by polarization-sensitive swept-source optical coherence tomography with 1- µm probe,” Opt. Express17(15), 12385–12396 (2009). [CrossRef] [PubMed]
  29. M. Yamanari, S. Makita, Y. Lim, and Y. Yasuno, “Full-range polarization-sensitive swept-source optical coherence tomography by simultaneous transversal and spectral modulation,” Opt. Express18(13), 13964–13980 (2010). [CrossRef] [PubMed]
  30. M. Miura, M. Yamanari, T. Iwasaki, M. Itoh, T. Yatagai, and Y. Yasuno, “Polarization-sensitive optical coherence tomography of necrotizing scleritis,” Ophthalmic Surg. Lasers Imaging40(6), 607–610 (2009). [CrossRef] [PubMed]
  31. S. Makita, M. Yamanari, and Y. Yasuno, “Generalized jones matrix optical coherence tomography: performance and local birefringence imaging,” Opt. Express18(2), 854–876 (2010). [CrossRef] [PubMed]
  32. L. Duan, S. Makita, M. Yamanari, Y. Lim, and Y. Yasuno, “Monte-carlo-based phase retardation estimator for polarization sensitive optical coherence tomography,” Opt. Express19(17), 16330–16345 (2011). [CrossRef] [PubMed]
  33. A. Alm and S. F. Nilsson, “Uveoscleral outflow--a review,” Exp. Eye Res.88(4), 760–768 (2009). [CrossRef] [PubMed]
  34. S. Sakai, M. Yamanari, Y. Lim, N. Nakagawa, and Y. Yasuno, “In vivo evaluation of human skin anisotropy by polarization-sensitive optical coherence tomography,” Biomed. Opt. Express2(9), 2623–2631 (2011). [CrossRef] [PubMed]
  35. T. W. Olsen, S. Sanderson, X. Feng, and W. C. Hubbard, “Porcine sclera: Thickness and surface area,” Invest. Ophthalmol. Vis. Sci.43(8), 2529–2532 (2002). [PubMed]
  36. B. K. Pierscionek, M. Asejczyk-Widlicka, and R. A. Schachar, “The effect of changing intraocular pressure on the corneal and scleral curvatures in the fresh porcine eye,” Br. J. Ophthalmol.91(6), 801–803 (2007). [CrossRef] [PubMed]
  37. D. S. Schultz, J. C. Lotz, S. M. Lee, M. L. Trinidad, and J. M. Stewart, “Structural factors that mediate scleral stiffness,” Invest. Ophthalmol. Vis. Sci.49(10), 4232–4236 (2008). [CrossRef] [PubMed]
  38. S. Nicoli, G. Ferrari, M. Quarta, C. Macaluso, P. Govoni, D. Dallatana, and P. Santi, “Porcine sclera as a model of human sclera for in vitro transport experiments: histology, sem, and comparative permeability,” Mol. Vis.15, 259–266 (2009). [PubMed]
  39. M. J. A. Girard, J.-K. F. Suh, M. Bottlang, C. F. Burgoyne, and J. C. Downs, “Biomechanical changes in the sclera of monkey eyes exposed to chronic iop elevations,” Invest. Ophthalmol. Vis. Sci.52(8), 5656–5669 (2011). [CrossRef] [PubMed]
  40. P. M. Pinsky, D. van der Heide, and D. Chernyak, “Computational modeling of mechanical anisotropy in the cornea and sclera,” J. Cataract Refract. Surg.31(1), 136–145 (2005). [CrossRef] [PubMed]
  41. R. Grytz and G. Meschke, “A computational remodeling approach to predict the physiological architecture of the collagen fibril network in corneo-scleral shells,” Biomech. Model. Mechanobiol.9(2), 225–235 (2010). [CrossRef] [PubMed]
  42. Collaborative Normal-Tension Glaucoma Study Group, “Comparison of glaucomatous progression between untreated patients with normal-tension glaucoma and patients with therapeutically reduced intraocular pressures,” Am. J. Ophthalmol.126(4), 487–497 (1998). [CrossRef] [PubMed]
  43. Y. Suzuki, A. Iwase, M. Araie, T. Yamamoto, H. Abe, S. Shirato, Y. Kuwayama, H. K. Mishima, H. Shimizu, G. Tomita, Y. Inoue, Y. Kitazawa, and Tajimi Study Group, “Risk factors for open-angle glaucoma in a japanese population: The tajimi study,” Ophthalmology113(9), 1613–1617 (2006). [CrossRef] [PubMed]
  44. M. J. A. Girard, J. C. Downs, C. F. Burgoyne, and J.-K. F. Suh, “Peripapillary and posterior scleral mechanics--part i: Development of an anisotropic hyperelastic constitutive model,” J. Biomech. Eng.131(5), 051011 (2009). [CrossRef] [PubMed]
  45. B. Coudrillier, C. Boote, H. A. Quigley, and T. D. Nguyen, “Scleral anisotropy and its effects on the mechanical response of the optic nerve head,” Biomech. Model. Mechanobiol.12(5), 941–963 (2013). [CrossRef] [PubMed]
  46. M. J. Hogan, J. A. Alvarado, and J. E. Weddell, Histology of the human eye: an atlas and textbook (Saunders, 1971).
  47. H. A. Quigley, E. M. Addicks, W. R. Green, and A. E. Maumenee, “Optic nerve damage in human glaucoma. Ii. the site of injury and susceptibility to damage,” Arch. Ophthalmol.99(4), 635–649 (1981). [CrossRef] [PubMed]
  48. Y. Lim, Y.-J. Hong, L. Duan, M. Yamanari, and Y. Yasuno, “Passive component based multifunctional jones matrix swept source optical coherence tomography for doppler and polarization imaging,” Opt. Lett.37(11), 1958–1960 (2012). [CrossRef] [PubMed]
  49. T. Torzicky, S. Marschall, M. Pircher, B. Baumann, M. Bonesi, S. Zotter, E. Götzinger, W. Trasischker, T. Klein, W. Wieser, B. Biedermann, R. Huber, P. Andersen, and C. K. Hitzenberger, “Retinal polarization-sensitive optical coherence tomography at 1060 nm with 350 khz a-scan rate using an fourier domain mode locked laser,” J. Biomed. Opt.18(2), 026008 (2013). [CrossRef] [PubMed]
  50. M. C. van Turnhout, S. Kranenbarg, and J. L. van Leeuwen, “Modeling optical behavior of birefringent biological tissues for evaluation of quantitative polarized light microscopy,” J. Biomed. Opt.14(5), 054018 (2009). [CrossRef] [PubMed]
  51. P. Watson and B. Hazleman, The Sclera and Systemic Disorders (Jp Medical Pub, 2012).
  52. R. H. Newton and K. M. Meek, “The integration of the corneal and limbal fibrils in the human eye,” Biophys. J.75(5), 2508–2512 (1998). [CrossRef] [PubMed]
  53. D. Yan, S. McPheeters, G. Johnson, U. Utzinger, and J. P. Vande Geest, “Microstructural differences in the human posterior sclera as a function of age and race,” Invest. Ophthalmol. Vis. Sci.52(2), 821–829 (2011). [CrossRef] [PubMed]
  54. M. J. A. Girard, A. Dahlmann-Noor, S. Rayapureddi, J. A. Bechara, B. M. E. Bertin, H. Jones, J. Albon, P. T. Khaw, and C. R. Ethier, “Quantitative mapping of scleral fiber orientation in normal rat eyes,” Invest. Ophthalmol. Vis. Sci.52(13), 9684–9693 (2011). [CrossRef] [PubMed]
  55. N. Morishige, A. J. Wahlert, M. C. Kenney, D. J. Brown, K. Kawamoto, T.-i. Chikama, T. Nishida, and J. V. Jester, “Second-harmonic imaging microscopy of normal human and keratoconus cornea,” Invest. Ophthalmol. Vis. Sci.48(3), 1087–1094 (2007). [CrossRef] [PubMed]
  56. J. M. Bueno, E. J. Gualda, A. Giakoumaki, P. Pérez-Merino, S. Marcos, and P. Artal, “Multiphoton microscopy of ex vivo corneas after collagen cross-linking,” Invest. Ophthalmol. Vis. Sci.52(8), 5325–5331 (2011). [CrossRef] [PubMed]
  57. N. Morishige, N. Yamada, X. Zhang, Y. Morita, N. Yamada, K. Kimura, A. Takahara, and K.-H. Sonoda, “Abnormalities of stromal structure in the bullous keratopathy cornea identified by second harmonic generation imaging microscopy,” Invest. Ophthalmol. Vis. Sci.53(8), 4998–5003 (2012). [CrossRef] [PubMed]
  58. M. Han, G. Giese, and J. Bille, “Second harmonic generation imaging of collagen fibrils in cornea and sclera,” Opt. Express13(15), 5791–5797 (2005). [CrossRef] [PubMed]
  59. S.-W. Teng, H.-Y. Tan, J.-L. Peng, H.-H. Lin, K. H. Kim, W. Lo, Y. Sun, W.-C. Lin, S.-J. Lin, S.-H. Jee, P. T. C. So, and C.-Y. Dong, “Multiphoton autofluorescence and second-harmonic generation imaging of the ex vivo porcine eye,” Invest. Ophthalmol. Vis. Sci.47(3), 1216–1224 (2006). [CrossRef] [PubMed]
  60. A. Miyazawa, M. Yamanari, S. Makita, M. Miura, K. Kawana, K. Iwaya, H. Goto, and Y. Yasuno, “Tissue discrimination in anterior eye using three optical parameters obtained by polarization sensitive optical coherence tomography,” Opt. Express17(20), 17426–17440 (2009). [CrossRef] [PubMed]
  61. L. Duan, M. Yamanari, and Y. Yasuno, “Automated phase retardation oriented segmentation of chorio-scleral interface by polarization sensitive optical coherence tomography,” Opt. Express20(3), 3353–3366 (2012). [CrossRef] [PubMed]
  62. T. Torzicky, M. Pircher, S. Zotter, M. Bonesi, E. Götzinger, and C. K. Hitzenberger, “Automated measurement of choroidal thickness in the human eye by polarization sensitive optical coherence tomography,” Opt. Express20(7), 7564–7574 (2012). [CrossRef] [PubMed]
  63. J. Liu and C. J. Roberts, “Influence of corneal biomechanical properties on intraocular pressure measurement,” J. Cataract Refract. Surg.31(1), 146–155 (2005). [CrossRef] [PubMed]

Cited By

Alert me when this paper is cited

OSA is able to provide readers links to articles that cite this paper by participating in CrossRef's Cited-By Linking service. CrossRef includes content from more than 3000 publishers and societies. In addition to listing OSA journal articles that cite this paper, citing articles from other participating publishers will also be listed.


« Previous Article  |  Next Article »

OSA is a member of CrossRef.

CrossCheck Deposited