OSA's Digital Library

Biomedical Optics Express

Biomedical Optics Express

  • Editor: Joseph A. Izatt
  • Vol. 4, Iss. 10 — Oct. 1, 2013
  • pp: 2051–2065

Pulsatile motion of the trabecular meshwork in healthy human subjects quantified by phase-sensitive optical coherence tomography

Peng Li, Tueng T. Shen, Murray Johnstone, and Ruikang K. Wang  »View Author Affiliations


Biomedical Optics Express, Vol. 4, Issue 10, pp. 2051-2065 (2013)
http://dx.doi.org/10.1364/BOE.4.002051


View Full Text Article

Enhanced HTML    Acrobat PDF (1813 KB)





Browse Journals / Lookup Meetings

Browse by Journal and Year


   


Lookup Conference Papers

Close Browse Journals / Lookup Meetings

Article Tools

Share
Citations

Abstract

Aqueous leaves the anterior chamber of eye by passing through the trabecular meshwork (TM), a tissue thought to be responsible for increased outflow resistance in glaucoma. Motion assessment could permit characterization of TM biomechanical properties necessary to maintain intra-ocular pressure (IOP) within a narrow homeostatic range. In this paper, we report the first in vivo identification of TM motion in humans. We use a phase-sensitive optical coherence tomography (PhS-OCT) system with sub-nanometer sensitivity to detect and image dynamic pulse-induced TM motion. To permit quantification of TM motion and relationships we develop and apply a phase compensation algorithm permitting removal of the otherwise evitable confounding effects of bulk motion. Twenty healthy human eyes from 10 subjects are imaged. The results permit visualization of pulsatile TM motion visualization by PhS-OCT; correlation with the digital/cardiac pulse is highly significant. The correlation permits assessment of the phase lag and time delay between TM motion and the cardiac pulse. In this study, we find that the digital pulse leads the pulsatile TM motion by a mean phase of 3.53 ± 0.48 rad and a mean time of 0.5 ± 0.14 s in the fundamental frequency. A significant linear relationship is present between the TM phase lag and the heart rate (p value < 0.05). The TM phase lag is also affected by age, the relationship not quite reaching significance in the current study. PhS-OCT reveals pulse-induced motion of the TM that may provide insights into the biomechanics of the tissues involved in the regulation of IOP.

© 2013 OSA

OCIS Codes
(170.0110) Medical optics and biotechnology : Imaging systems
(170.3880) Medical optics and biotechnology : Medical and biological imaging
(170.4470) Medical optics and biotechnology : Ophthalmology
(170.4500) Medical optics and biotechnology : Optical coherence tomography

ToC Category:
Ophthalmology Applications

History
Original Manuscript: June 11, 2013
Revised Manuscript: July 29, 2013
Manuscript Accepted: July 30, 2013
Published: September 6, 2013

Citation
Peng Li, Tueng T. Shen, Murray Johnstone, and Ruikang K. Wang, "Pulsatile motion of the trabecular meshwork in healthy human subjects quantified by phase-sensitive optical coherence tomography," Biomed. Opt. Express 4, 2051-2065 (2013)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-4-10-2051


Sort:  Author  |  Year  |  Journal  |  Reset  

References

  1. L. S. Wilson, D. E. Robinson, and M. J. Dadd, “Elastography--the movement begins,” Phys. Med. Biol.45(6), 1409–1421 (2000). [CrossRef] [PubMed]
  2. J. F. Greenleaf, M. Fatemi, and M. Insana, “Selected methods for imaging elastic properties of biological tissues,” Annu. Rev. Biomed. Eng.5(1), 57–78 (2003). [CrossRef] [PubMed]
  3. J. Ophir, S. Alam, B. Garra, F. Kallel, E. Konofagou, T. Krouskop, C. Merritt, R. Righetti, R. Souchon, S. Srinivasan, and T. Varghese, “Elastography: Imaging the elastic properties of soft tissues with ultrasound,” J. Med. Ultrasound29(4), 155–171 (2002). [CrossRef]
  4. R. J. Dickinson and C. R. Hill, “Measurement of soft tissue motion using correlation between A-scans,” Ultrasound Med. Biol.8(3), 263–271 (1982). [CrossRef] [PubMed]
  5. D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991). [CrossRef] [PubMed]
  6. P. H. Tomlins and R. K. Wang, “Theory, developments and applications of optical coherence tomography,” J. Phys. D Appl. Phys.38(15), 2519–2535 (2005). [CrossRef]
  7. A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys.66(2), 239–303 (2003). [CrossRef]
  8. J. Schmitt, “OCT elastography: imaging microscopic deformation and strain of tissue,” Opt. Express3(6), 199–211 (1998). [CrossRef] [PubMed]
  9. R. Chan, A. Chau, W. Karl, S. Nadkarni, A. Khalil, N. Iftimia, M. Shishkov, G. Tearney, M. Kaazempur-Mofrad, and B. Bouma, “OCT-based arterial elastography: robust estimation exploiting tissue biomechanics,” Opt. Express12(19), 4558–4572 (2004). [CrossRef] [PubMed]
  10. J. Rogowska, N. A. Patel, J. G. Fujimoto, and M. E. Brezinski, “Optical coherence tomographic elastography technique for measuring deformation and strain of atherosclerotic tissues,” Heart90(5), 556–562 (2004). [CrossRef] [PubMed]
  11. R. K. Wang, Z. Ma, and S. J. Kirkpatrick, “Tissue Doppler optical coherence elastography for real time strain rate and strain mapping of soft tissue,” Appl. Phys. Lett.89(14), 144103 (2006). [CrossRef]
  12. R. K. Wang, S. Kirkpatrick, and M. Hinds, “Phase-sensitive optical coherence elastography for mapping tissue microstrains in real time,” Appl. Phys. Lett.90(16), 164105 (2007). [CrossRef]
  13. X. Liang, A. L. Oldenburg, V. Crecea, E. J. Chaney, and S. A. Boppart, “Optical micro-scale mapping of dynamic biomechanical tissue properties,” Opt. Express16(15), 11052–11065 (2008). [CrossRef] [PubMed]
  14. X. Liang, S. G. Adie, R. John, and S. A. Boppart, “Dynamic spectral-domain optical coherence elastography for tissue characterization,” Opt. Express18(13), 14183–14190 (2010). [CrossRef] [PubMed]
  15. P. Li, A. Liu, L. Shi, X. Yin, S. Rugonyi, and R. K. Wang, “Assessment of strain and strain rate in embryonic chick heart in vivo using tissue Doppler optical coherence tomography,” Phys. Med. Biol.56(22), 7081–7092 (2011). [CrossRef] [PubMed]
  16. P. Li, X. Yin, L. Shi, S. Rugonyi, and R. K. Wang, “In vivo functional imaging of blood flow and wall strain rate in outflow tract of embryonic chick heart using ultrafast spectral domain optical coherence tomography,” J. Biomed. Opt.17(9), 096006 (2012). [CrossRef] [PubMed]
  17. R. K. Wang and A. L. Nuttall, “Phase-sensitive optical coherence tomography imaging of the tissue motion within the organ of Corti at a subnanometer scale: a preliminary study,” J. Biomed. Opt.15(5), 056005 (2010). [CrossRef] [PubMed]
  18. P. Li, R. Reif, Z. Zhi, E. Martin, T. T. Shen, M. Johnstone, and R. K. Wang, “Phase-sensitive optical coherence tomography characterization of pulse-induced trabecular meshwork displacement in ex vivo nonhuman primate eyes,” J. Biomed. Opt.17(7), 076026 (2012). [CrossRef] [PubMed]
  19. S. G. Adie, X. Liang, B. F. Kennedy, R. John, D. D. Sampson, and S. A. Boppart, “Spectroscopic optical coherence elastography,” Opt. Express18(25), 25519–25534 (2010). [CrossRef] [PubMed]
  20. C. Sun, B. Standish, and V. X. Yang, “Optical coherence elastography: current status and future applications,” J. Biomed. Opt.16(4), 043001 (2011). [CrossRef] [PubMed]
  21. Y. Zhao, Z. Chen, Z. Ding, H. Ren, and J. S. Nelson, “Real-time phase-resolved functional optical coherence tomography by use of optical Hilbert transformation,” Opt. Lett.27(2), 98–100 (2002). [CrossRef] [PubMed]
  22. R. K. Wang and Z. Ma, “Real-time flow imaging by removing texture pattern artifacts in spectral-domain optical Doppler tomography,” Opt. Lett.31(20), 3001–3003 (2006). [CrossRef] [PubMed]
  23. P. Li, L. An, G. Lan, M. Johnstone, D. Malchow, and R. K. Wang, “Extended imaging depth to 12 mm for 1050-nm spectral domain optical coherence tomography for imaging the whole anterior segment of the human eye at 120-kHz A-scan rate,” J. Biomed. Opt.18(1), 016012 (2013). [CrossRef] [PubMed]
  24. C. I. Phillips, S. Tsukahara, O. Hosaka, and W. Adams, “Ocular pulsation correlates with ocular tension: the choroid as piston for an aqueous pump?” Ophthalmic Res.24(6), 338–343 (1992). [CrossRef] [PubMed]
  25. P. L. Kaufman and C. A. Rasmussen, “Advances in glaucoma treatment and management: outflow drugs,” Invest. Ophthalmol. Vis. Sci.53(5), 2495–2500 (2012). [CrossRef] [PubMed]
  26. R. F. Ramos and W. D. Stamer, “Effects of cyclic intraocular pressure on conventional outflow facility,” Invest. Ophthalmol. Vis. Sci.49(1), 275–281 (2008). [CrossRef] [PubMed]
  27. R. F. Ramos, G. M. Sumida, and W. D. Stamer, “Cyclic mechanical stress and trabecular meshwork cell contractility,” Invest. Ophthalmol. Vis. Sci.50(8), 3826–3832 (2009). [CrossRef] [PubMed]
  28. S. J. Tumminia, K. P. Mitton, J. Arora, P. Zelenka, D. L. Epstein, and P. Russell, “Mechanical stretch alters the actin cytoskeletal network and signal transduction in human trabecular meshwork cells,” Invest. Ophthalmol. Vis. Sci.39(8), 1361–1371 (1998). [PubMed]
  29. C. Luna, G. Li, P. B. Liton, D. L. Epstein, and P. Gonzalez, “Alterations in gene expression induced by cyclic mechanical stress in trabecular meshwork cells,” Mol. Vis.15, 534–544 (2009). [PubMed]
  30. P. B. Liton, X. Liu, P. Challa, D. L. Epstein, and P. Gonzalez, “Induction of TGF-beta1 in the trabecular meshwork under cyclic mechanical stress,” J. Cell. Physiol.205(3), 364–371 (2005). [CrossRef] [PubMed]
  31. P. B. Liton, C. Luna, M. Bodman, A. Hong, D. L. Epstein, and P. Gonzalez, “Induction of IL-6 expression by mechanical stress in the trabecular meshwork,” Biochem. Biophys. Res. Commun.337(4), 1229–1236 (2005). [CrossRef] [PubMed]
  32. E. R. Tamm, P. Russell, D. L. Epstein, D. H. Johnson, and J. Piatigorsky, “Modulation of myocilin/TIGR expression in human trabecular meshwork,” Invest. Ophthalmol. Vis. Sci.40(11), 2577–2582 (1999). [PubMed]
  33. K. P. Mitton, S. J. Tumminia, J. Arora, P. Zelenka, D. L. Epstein, and P. Russell, “Transient loss of alphaB-crystallin: an early cellular response to mechanical stretch,” Biochem. Biophys. Res. Commun.235(1), 69–73 (1997). [CrossRef] [PubMed]
  34. B. Junglas, S. Kuespert, A. A. Seleem, T. Struller, S. Ullmann, M. Bösl, A. Bosserhoff, J. Köstler, R. Wagner, E. R. Tamm, and R. Fuchshofer, “Connective tissue growth factor causes glaucoma by modifying the actin cytoskeleton of the trabecular meshwork,” Am. J. Pathol.180(6), 2386–2403 (2012). [CrossRef] [PubMed]
  35. C. Luna, G. Li, J. Qiu, P. Challa, D. L. Epstein, and P. Gonzalez, “Extracellular release of ATP mediated by cyclic mechanical stress leads to mobilization of AA in trabecular meshwork cells,” Invest. Ophthalmol. Vis. Sci.50(12), 5805–5810 (2009). [CrossRef] [PubMed]
  36. J. M. B. Bradley, M. J. Kelley, A. Rose, and T. S. Acott, “Signaling Pathways Used in Trabecular Matrix Metalloproteinase Response to Mechanical Stretch,” Invest. Ophthalmol. Vis. Sci.44(12), 5174–5181 (2003). [CrossRef] [PubMed]
  37. V. Vittal, A. Rose, K. E. Gregory, M. J. Kelley, and T. S. Acott, “Changes in gene expression by trabecular meshwork cells in response to mechanical stretching,” Invest. Ophthalmol. Vis. Sci.46(8), 2857–2868 (2005). [CrossRef] [PubMed]
  38. T. S. Acott and M. J. Kelley, “Extracellular matrix in the trabecular meshwork,” Exp. Eye Res.86(4), 543–561 (2008). [CrossRef] [PubMed]
  39. K. E. Keller, M. Aga, J. M. Bradley, M. J. Kelley, and T. S. Acott, “Extracellular matrix turnover and outflow resistance,” Exp. Eye Res.88(4), 676–682 (2009). [CrossRef] [PubMed]
  40. W. D. Stamer and T. S. Acott, “Current understanding of conventional outflow dysfunction in glaucoma,” Curr. Opin. Ophthalmol.23(2), 135–143 (2012). [CrossRef] [PubMed]
  41. D. WuDunn, “The effect of mechanical strain on matrix metalloproteinase production by bovine trabecular meshwork cells,” Curr. Eye Res.22(5), 394–397 (2001). [CrossRef] [PubMed]
  42. J. M. Bradley, M. J. Kelley, X. Zhu, A. M. Anderssohn, J. P. Alexander, and T. S. Acott, “Effects of mechanical stretching on trabecular matrix metalloproteinases,” Invest. Ophthalmol. Vis. Sci.42(7), 1505–1513 (2001). [PubMed]
  43. K. E. Keller, M. J. Kelley, and T. S. Acott, “Extracellular matrix gene alternative splicing by trabecular meshwork cells in response to mechanical stretching,” Invest. Ophthalmol. Vis. Sci.48(3), 1164–1172 (2007). [CrossRef] [PubMed]
  44. M. A. Johnstone, “The aqueous outflow system as a mechanical pump: evidence from examination of tissue and aqueous movement in human and non-human primates,” J. Glaucoma13(5), 421–438 (2004). [CrossRef] [PubMed]
  45. E. H. Zhou, R. Krishnan, W. D. Stamer, K. M. Perkumas, K. Rajendran, J. F. Nabhan, Q. Lu, J. J. Fredberg, and M. Johnson, “Mechanical responsiveness of the endothelial cell of Schlemm’s canal: scope, variability and its potential role in controlling aqueous humour outflow,” J. R. Soc. Interface9(71), 1144–1155 (2012). [CrossRef] [PubMed]
  46. R. Clark, A. Nosie, T. Walker, J. A. Faralli, M. S. Filla, G. Barrett-Wilt, and D. M. Peters, “Comparative genomic and proteomic analysis of cytoskeletal changes in dexamethasone-treated trabecular meshwork cells,” Mol. Cell. Proteomics12(1), 194–206 (2013). [CrossRef] [PubMed]
  47. M. S. Filla, M. K. Schwinn, A. K. Nosie, R. W. Clark, and D. M. Peters, “Dexamethasone-associated cross-linked actin network formation in human trabecular meshwork cells involves β3 integrin signaling,” Invest. Ophthalmol. Vis. Sci.52(6), 2952–2959 (2011). [CrossRef] [PubMed]
  48. S. O’Reilly, N. Pollock, L. Currie, L. Paraoan, A. F. Clark, and I. Grierson, “Inducers of cross-linked actin networks in trabecular meshwork cells,” Invest. Ophthalmol. Vis. Sci.52(10), 7316–7324 (2011). [CrossRef] [PubMed]
  49. J. A. Last, T. Pan, Y. Ding, C. M. Reilly, K. Keller, T. S. Acott, M. P. Fautsch, C. J. Murphy, and P. Russell, “Elastic modulus determination of normal and glaucomatous human trabecular meshwork,” Invest. Ophthalmol. Vis. Sci.52(5), 2147–2152 (2011). [CrossRef] [PubMed]
  50. P. Russell and M. Johnson, “Elastic modulus determination of normal and glaucomatous human trabecular meshwork,” Invest. Ophthalmol. Vis. Sci.53(1), 117 (2012). [CrossRef]
  51. S. M. Thomasy, J. A. Wood, P. H. Kass, C. J. Murphy, and P. Russell, “Substratum stiffness and latrunculin B regulate matrix gene and protein expression in human trabecular meshwork cells,” Invest. Ophthalmol. Vis. Sci.53(2), 952–958 (2012). [CrossRef] [PubMed]
  52. M. Johnstone, E. Martin, and A. Jamil, “Pulsatile flow into the aqueous veins: Manifestations in normal and glaucomatous eyes,” Exp. Eye Res.92(5), 318–327 (2011). [CrossRef] [PubMed]
  53. M. A. Johnstone, “A New Model Describes an Aqueous Outflow Pump and Explores Causes of Pump Failure in Glaucoma,” in Glaucoma. Essentials in Ophthalmology, F. Grehn and R. Stamper, eds. (Springer Berlin Heidelberg, 2006), pp. 3–34.
  54. E. B. Suson and R. O. Schultz, “Blood in schlemm’s canal in glaucoma suspects. A study of the relationship between blood-filling pattern and outflow facility in ocular hypertension,” Arch. Ophthalmol.81(6), 808–812 (1969). [CrossRef] [PubMed]
  55. B. A. Francis, K. Singh, S. C. Lin, E. Hodapp, H. D. Jampel, J. R. Samples, and S. D. Smith, “Novel glaucoma procedures: a report by the American Academy of Ophthalmology,” Ophthalmology118(7), 1466–1480 (2011). [PubMed]
  56. H. Saheb and I. I. Ahmed, “Micro-invasive glaucoma surgery: current perspectives and future directions,” Curr. Opin. Ophthalmol.23(2), 96–104 (2012). [CrossRef] [PubMed]
  57. M. P. Fautsch and D. H. Johnson, “Aqueous humor outflow: what do we know? Where will it lead us?” Invest. Ophthalmol. Vis. Sci.47(10), 4181–4187 (2006). [CrossRef] [PubMed]
  58. R. K. Wang and Z. Ma, “A practical approach to eliminate autocorrelation artefacts for volume-rate spectral domain optical coherence tomography,” Phys. Med. Biol.51(12), 3231–3239 (2006). [CrossRef] [PubMed]
  59. American National Standard Institute, Safe use of lasers and safe use of optical fiber communications. New York: ANSI, Z136 committee; 2000:168.
  60. S. Makita, Y. Hong, M. Yamanari, T. Yatagai, and Y. Yasuno, “Optical coherence angiography,” Opt. Express14(17), 7821–7840 (2006). [CrossRef] [PubMed]
  61. L. An, T. T. Shen, and R. K. Wang, “Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina,” J. Biomed. Opt.16(10), 106013 (2011). [CrossRef] [PubMed]
  62. S. Asrani, M. Sarunic, C. Santiago, and J. Izatt, “Detailed visualization of the anterior segment using fourier-domain optical coherence tomography,” Arch. Ophthalmol.126(6), 765–771 (2008). [CrossRef] [PubMed]
  63. C. G. Caro and D. A. McDONALD, “The relation of pulsatile pressure and flow in the pulmonary vascular bed,” J. Physiol.157, 426–453 (1961). [PubMed]
  64. S. Solomon, S. D. Katz, W. Stevenson-Smith, E. L. Yellin, and T. H. LeJemtel, “Determination of vascular impedance in the peripheral circulation by transcutaneous pulsed Doppler ultrasound,” Chest108(2), 515–521 (1995). [CrossRef] [PubMed]
  65. M. F. O’Rourke, “Pressure and flow waves in systemic arteries and the anatomical design of the arterial system,” J. Appl. Physiol.23(2), 139–149 (1967). [PubMed]
  66. D. A. McDonald, “The relation of pulsatile pressure to flow in arteries,” J. Physiol.127(3), 533–552 (1955). [PubMed]
  67. J. R. Womersley, “Method for the calculation of velocity, rate of flow and viscous drag in arteries when the pressure gradient is known,” J. Physiol.127(3), 553–563 (1955). [PubMed]
  68. D. J. Patel, J. C. Greenfield, W. G. Austen, A. G. Morrow, and D. L. Fry, “Pressure-flow relationships in the ascending aorta and femoral artery of man,” J. Appl. Physiol.20(3), 459–463 (1965). [PubMed]
  69. M. F. O'Rourke and M. G. Taylor, “Vascular Impedance of the Femoral Bed,” Circ. Res.18(2), 126–139 (1966). [CrossRef]
  70. M. F. O’Rourke and M. G. Taylor, “Input impedance of the systemic circulation,” Circ. Res.20(4), 365–380 (1967). [CrossRef] [PubMed]
  71. R. K. Wang and L. An, “Multifunctional imaging of human retina and choroid with 1050-nm spectral domain optical coherence tomography at 92-kHz line scan rate,” J. Biomed. Opt.16(5), 050503 (2011). [CrossRef] [PubMed]
  72. L. An, P. Li, G. Lan, D. Malchow, and R. K. Wang, “High-resolution 1050 nm spectral domain retinal optical coherence tomography at 120 kHz A-scan rate with 6.1 mm imaging depth,” Biomed. Opt. Express4(2), 245–259 (2013). [CrossRef] [PubMed]
  73. R. N. Weinreb and P. L. Kaufman, “Glaucoma research community and FDA look to the future, II: NEI/FDA Glaucoma Clinical Trial Design and Endpoints Symposium: measures of structural change and visual function,” Invest. Ophthalmol. Vis. Sci.52(11), 7842–7851 (2011). [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