Background. Scleral biomechanical properties may be important in the pathogenesis and progression of glaucoma. The goal of this study is to develop and validate an ultrasound method for measuring cross-sectional distributive strains in the sclera during elevations of intraocular pressure (IOP). Method of Approach. Porcine globes (n = 5) were tested within 24 hs postmortem. The posterior scleral shells were dissected and mounted onto a custom-built pressurization chamber. A high-frequency (55-MHz) ultrasound system (Vevo660, VisualSonics Inc., Toronto) was employed to acquire the radio frequency data during scans of the posterior pole along both circumferential and meridian directions. The IOP was gradually increased from 5 to 45 mmHg. The displacement fields were obtained from correlation-based ultrasound speckle tracking. A least-square strain estimator was used to calculate the strains in both axial and lateral directions. Experimental validation was performed by comparing tissue displacements calculated from ultrasound speckle tracking with those induced by an actuator. Theoretical analysis and simulation experiments were performed to optimize the ultrasound speckle tracking method and evaluate the accuracy and signal-to-noise ratio (SNR) in strain estimation. Results. Porcine sclera exhibited significantly larger axial strains (e.g., −5.1 ± 1.5% at 45 mmHg, meridian direction) than lateral strains (e.g., 2.2 ± 0.7% at 45 mmHg, meridian direction) during IOP elevations (P’s < 0.01). The strain magnitudes increased nonlinearly with pressure increase. The strain maps displayed heterogeneity through the thickness. The lateral strains were significantly smaller in the circumferential direction than the meridian direction at 45 mmHg (P < 0.05). Experimental validation showed that the ultrasound speckle tracking method was capable of tracking displacements at the accuracy of sub-micron to micron. Theoretical analysis predicted the dependence of the strain estimation SNR on the strain level, as well as signal processing parameters such as kernel size. Simulation results showed that ultrasound speckle tracking had a high accuracy for estimating strains of 1–5% and a high SNR for strains of 0.5–5%. Conclusions. A new experimental method based on ultrasound speckle tracking has been developed for obtaining cross-sectional strain maps of the posterior sclera. This method provides a useful tool to examine distributive strains through the thickness of the sclera during elevations of IOP.
Issue Section:
Research Papers
References
1.
Kingman
, S.
, 2004, “Glaucoma is Second Leading Cause of Blindness Globally
,” Bull. World Health Organ.
, 82
(11
), pp. 887
–888
. Available at http://www.scielosp.org/pdf/bwho/v82n11/v82n11a19.pdf2.
Burgoyne
, C. F.
, Downs
, J. C.
, Bellezza
, A. J.
, Suh
, J. K. F.
, and Hart
, R. T.
, 2005, “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
), pp. 39
–73
.3.
Sigal
, I. A.
, Flanagan
, J. G.
, and Ethier
, C. R.
, 2005, “Factors Influencing Optic Nerve Head Biomechanics
,” Invest. Ophthalmol. Visual Sci.
, 46
(11
), pp. 4189
–4199
.4.
Sigal
, I. A.
, Flanagan
, J. G.
, Tertinegg
, I.
, and Ethier
, C. R.
, 2009, “Modeling Individual-Specific Human Optic Nerve Head Biomechanics. Part II: Influence of Material Properties
,” Biomech. Model. Mechanobiol.
, 8
(2
), pp. 99
–109
.5.
McBrien
, N. A.
, Cornell
, L. M.
, and Gentle
, A.
, 2001, “Structural and Ultrastructural Changes to the Sclera in a Mammalian Model of High Myopia
,” Invest. Ophthalmol. Visual Sci.
, 42
(10
), pp. 2179
–2187
. Available at http://www.ncbi.nlm.nih.gov/pubmed/115279286.
Phillips
, J. R.
, and Mcbrien
, N. A.
, 1995, “Form Deprivation Myopia – Elastic Properties of Sclera
,” Ophthalmic Physiol. Opt.
, 15
(5
), pp. 357
–362
.7.
Siegwart
, J. T.
, and Norton
, T. T.
, 1999, “Regulation of the Mechanical Properties of Tree Shrew Sclera by the Visual Environment
,” Vision Res.
, 39
(2
), pp. 387
–407
.8.
McBrien
, N. A.
, Jobling
, A. I.
, and Gentle
, A.
, 2009, “Biomechanics of the Sclera in Myopia: Extracellular and Cellular Factors
,” Optom. Vision Sci.
, 86
(1
), pp. 23
–30
.9.
Mitchell
, P.
, Hourihan
, F.
, Sandbach
, J.
, and Wang
, J. J.
, 1999, “The Relationship Between Glaucoma and Myopia – The Blue Mountains Eye Study
,” Ophthalmology
, 106
(10
), pp. 2010
–2015
.10.
Watson
, P. G.
, and Young
, R. D.
, 2004, “Scleral Structure, Organisation and Disease. A Review
,” Exp. Eye Res.
, 78
(3
), pp. 609
–623
.11.
Friberg
, T. R.
, and Lace
, J. W.
, 1988, “A Comparison of the Elastic Properties of Human Choroid and Sclera
,” Exp. Eye Res.
, 47
(3
), pp. 429
–436
.12.
Elsheikh
, A.
, Geraghty
, B.
, Alhasso
, D.
, Knappett
, J.
, Campanelli
, M.
, and Rama
, P.
, 2010, “Regional Variation in the Biomechanical Properties of the Human Sclera
,” Exp. Eye Res.
, 90
(5
), pp. 624
–633
.13.
Downs
, J. C.
, Suh
, J. K. F.
, Thomas
, K. A.
, Bellezza
, A. J.
, Hart
, R. T.
, and Burgoyne
, C. F.
, 2005, “Viscoelastic Material Properties of the Peripapillary Sclera in Normal and Early-Glaucoma Monkey Eyes
,” Invest. Ophthalmol. Visual Sci.
, 46
(2
), pp. 540
–546
.14.
Schultz
, D. S.
, Lotz
, J. C.
, Lee
, S. M.
, Trinidad
, M. L.
, and Stewart
, J. M.
, 2008, “Structural Factors That Mediate Scleral Stiffness
,” Invest. Ophthalmol. Visual Sci.
, 49
(10
), pp. 4232
–4236
.15.
Palko
, J. R.
, Pan
, X. L.
, and Liu
, J.
, 2011, “Dynamic Testing of Regional Viscoelastic Behavior of Canine Sclera
,” Exp. Eye Res.
, 93
(6
), pp. 825
–832
.16.
Curtin
, B. J.
, 1969, “Physiopathologic Aspects of Scleral Stress-Strain
,” Trans. Am. Ophthalmol. Soc.
, 67
, pp. 417
–461
.17.
Eilaghi
, A.
, Flanagan
, J. G.
, Tertinegg
, I.
, Simmons
, C. A.
, Brodland
, G. W.
, and Ethier
, C. R.
, 2010, “Biaxial Mechanical Testing of Human Sclera
,” J. Biomechanics
, 43
(9
), pp. 1696
–1701
.18.
Mortazavi
, A. M.
, Simon
, B. R.
, Stamer
, W. D.
, and Geest
, J. P. V.
, 2009, “Drained Secant Modulus for Human and Porcine Peripapillary Sclera Using Unconfined Compression Testing
,” Exp. Eye Res.
, 89
(6
), pp. 892
–897
.19.
Battaglioli
, J. L.
, and Kamm
, R. D.
, 1984, “Measurements of the Compressive Properties of Scleral Tissue
,” Invest. Ophthalmol. Visual Sci.
, 25
(1
), pp. 59
–65
.20.
Woo
, S. L -Y L-Y
., Kobayashi
, A. S.
, Schlegela
, W. A.
, and Lawrence
, C.
, 1972, “Nonlinear Material Properties of Intact Cornea and Sclera
,” Exp. Eye Res.
, 14
(1
), pp. 29
–39
.21.
Girard
, M. J. A.
, Downs
, J. C.
, Burgoyne
, C. F.
, and Suh
, J. K. F.
, 2008, “Experimental Surface Strain Mapping of Porcine Peripapillary Sclera due to Elevations of Intraocular Pressure
,” ASME J. Biomech. Eng.
, 130
(4
), p. 041017
.22.
Myers
, K. M.
, Cone
, F. E.
, Quigley
, H. A.
, Gelman
, S.
, Pease
, M. E.
, and Nguyen
, T. D.
, 2010, “The In Vitro Inflation Response of Mouse Sclera
,” Exp. Eye Res.
, 91
(6
), pp. 866
–875
.23.
Myers
, K. M.
, Coudrillier
, B.
, Boyce
, B. L.
, and Nguyen
, T. D.
, 2010, “The Inflation Response of the Posterior Bovine Sclera
,” Acta Biomater.
, 6
(11
), pp. 4327
–4335
.24.
Greene
, P. R.
, and Mcmahon
, T. A.
, 1979, “Scleral Creep Vs Temperature and Pressure in vitro
,” Exp. Eye Res.
, 29
(5
), pp. 527
–537
.25.
Girard
, M. J. A.
, Downs
, J. C.
, Bottlang
, M.
, Burgoyne
, C. F.
, and Suh
, J. K. F.
, 2009, “Peripapillary and Posterior Scleral Mechanics-Part II: Experimental and Inverse Finite Element Characterization
,” ASME J. Biomech. Eng.
, 131
(5
), p. 051011
.26.
Girard
, M. J. A.
, Downs
, J. C.
, Burgoyne
, C. F.
, and Suh
, J. K. F.
, 2009, “Peripapillary and Posterior Scleral Mechanics-Part I: Development of an Anisotropic Hyperelastic Constitutive Model
,” ASME J. Biomech. Eng.
, 131
(5
), p. 051012
.27.
Ophir
, J.
, Cespedes
, I.
, Ponnekanti
, H.
, Yazdi
, Y.
, and Li
, X.
, 1991, “Elastography – A Quantitative Method for Imaging the Elasticity of Biological Tissues
,” Ultrason. Imaging
, 13
(2
), pp. 111
–134
.28.
Odonnell
, M.
Skovoroda
, A. R.
Shapo
, B. M.
and Emelianov
, S. Y.
, 1994, “Internal Displacement and Strain Imaging Using Ultrasonic Speckle Tracking
,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control
, 41
(3
), pp. 314
–325
.29.
Krouskop
, T. A.
, Wheeler
, T. M.
, Kallel
, F.
, Garra
, B. S.
, and Hall
, T.
, 1998, “Elastic Moduli of Breast and Prostate Tissues under Compression
,” Ultrason. Imaging
, 20
(4
), pp. 260
–274
. Available at http://www.ncbi.nlm.nih.gov/pubmed/1019734730.
Suffoletto
, M. S.
, Dohi
, K.
, Cannesson
, M.
, Saba
, S.
, and Gorcsan
, J.
, 2006, “Novel Speckle-Tracking Radial Strain From Routine Black-and-White Echocardiographic Images to Quantify Dyssynchrony and Predict Response to Cardiac Resynchronization Therapy
,” Circulation
, 113
(7
), pp. 960
–968
.31.
Ryan
, L. K.
, and Foster
, F. S.
, 1997, “Ultrasonic Measurement of Differential Displacement Strain in a Vascular Model
,” Ultrason. Imaging
, 19
(1
), pp. 19
–38
.32.
Righetti
, R.
, Kallel
, F.
, Stafford
, R. J.
, Price
, R. E.
, Krouskop
, T. A.
, Hazle
, J. D.
, and Ophir
, J.
, 1999, “Elastographic Characterization of HIFU-Induced Lesions in Canine Livers
,” Ultrasound in Med. Biol.
, 25
(7
), pp. 1099
–1113
.33.
Kallel
, F.
, Ophir
, J.
, Magee
, K.
, and Krouskop
, T.
, 1998, “Elastographic Imaging of Low-Contrast Elastic Modulus Distributions in Tissue
,” Ultrasound Med. Biol.
, 24
(3
), pp. 409
–425
.34.
Kallel
, F.
, Price
, R. E.
, Konofagou
, E.
, and Ophir
, J.
, 1999, “Elastographic Imaging of the Normal Canine Prostate In Vitro
,” Ultrason. Imaging
, 21
(3
), pp. 201
–215
.35.
Bohs
, L. N.
, and Trahey
, G. E.
, 1991, “A Novel Method for Angle Independent Ultrasonic-Imaging of Blood-Flow and Tissue Motion
,” IEEE Trans. Biomed. Eng.
, 38
(3
), pp. 280
–286
.36.
Angelini
, E. D.
, and Gerard
, O.
, 2006, “Review of Myocardial Motion Estimation Methods From Optical Flow Tracking on Ultrasound Data
,” 2006 28th Annual International Conference of the IEEE Engineering in Medicine and Biology Society
, Vols. 1–15, pp. 6337–6340.37.
Kallel
, F.
, and Ophir
, J.
, 1997, “A Least-Squares Strain Estimator for Elastography
,” Ultrason. Imaging
, 19
(3
), pp. 195
–208
. Available at http://www.ncbi.nlm.nih.gov/pubmed/944766838.
Nightingale
, K. R.
, Palmeri
, M. L.
, Nightingale
, R. W.
, and Trahey
, G. E.
, 2001, “On the Feasibility of Remote Palpation Using Acoustic Radiation Force
,” J. Acoust. Soc. Am.
, 110
(1
), pp. 625
–634
.39.
Konofagou
, E. E.
, and Hynynen
, K.
, 2003, “Localized Harmonic Motion Imaging: Theory, Simulations and Experiments
,” Ultrasound Med. Biol.
, 29
(10
), pp. 1405
–1413
.40.
Srinivasan
, S.
, Righetti
, R.
, and Ophir
, J.
, 2003, “Trade-offs Between the Axial Resolution and the Signal-to-Noise Ratio in Elastography
,” Ultrasound Med. Biol.
, 29
(6
), pp. 847
–866
.41.
Varghese
, T.
, and Ophir
, J.
, 1997, “A Theoretical Framework for Performance Characterization of Elastography: The Strain Filter
,” IEEE Trans. Ultrason.Ferroelectr. Freq. Control
, 44
(1
), pp. 164
–172
.42.
Skovoroda
, A. R.
, Emelianov
, S. Y.
, Lubinski
, M. A.
, Sarvazyan
, A. P.
, and Odonnell
, M.
, 1994, “Theoretical-Analysis and Verification of Ultrasound Displacement and Strain Imaging
,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control
, 41
(3
), pp. 302
–313
.43.
Varghese
, T.
, Bilgen
, M.
, and Ophir
, J.
, 1998, “Multiresolution Imaging in Elastography
,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control
, 45
(1
), pp. 65
–75
.44.
Varghese
, T.
, Ophir
, J.
, Konofagou
, E.
, Kallel
, F.
, and Righetti
, R.
, 2001, “Tradeoffs in Elastographic Imaging
,” Ultrason. Imaging
, 23
(4
), pp. 216
–248
. Available at http://www.ncbi.nlm.nih.gov/pubmed/1205127645.
Hollman
, K. W.
, Emelianov
, S. Y.
, Neiss
, J. H.
, Jotyan
, G.
, Spooner
, G. J. R.
, Juhasz
, T.
, Kurtz
, R. M.
, and O’Donnell
, M.
, 2002, “Strain Imaging of Corneal Tissue with an Ultrasound Elasticity Microscope
,” Cornea
, 21
(1
), pp. 68
–73
.46.
Ford
, M. R.
, Dupps
, W. J.
, Rollins
, A. M.
, Roy
, A. S.
, and Hu
, Z. L.
, 2011, “Method for Optical Coherence Elastography of the Cornea
,” J. Biomed. Optics
, 16
(1
), p. 016005
.47.
Cohn
, N. A.
, Emelianov
, S. Y.
, Lubinski
, M. A.
, and ODonnell
, M.
, 1997, “An Elasticity Microscope. 1. Methods
,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control
, 44
(6
), pp. 1304
–1319
.48.
Weinstein
, E.
, and Weiss
, A. J.
, 1984, “Fundamental Limitations in Passive Time-Delay Estimation. 2. Wideband Systems
,” IEEE Trans. Acoust., Speech, Signal Process.
, 32
(5
), pp. 1064
–1078
.49.
Jensen
, J. A.
, 1996, “Field: A Program for Simulating Ultrasound Systems
,” 10th Nordicbaltic Conference on Biomedical Imaging, Vol. 4(1), pp. 351
–353
.50.
Jensen
, J. A.
, and Svendsen
, N. B.
, 1992, “Calculation of Pressure Fields from Arbitrarily Shaped, Apodized, and Excited Ultrasound Transducers
,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control
, 39
(2
), pp. 262
–267
.51.
Zagzebski
, J. A.
, Chen
, J. F.
, Dong
, F.
, and Wilson
, T.
, 1999, “Intervening Attenuation Affects First-Order Statistical Properties of Ultrasound Echo Signals
,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control
, 46
(1
), pp. 35
–40
.52.
Komai
, Y.
, and Ushiki
, T.
, 1991, “The 3-Dimensional Organization of Collagen Fibrils in the Human Cornea and Sclera
,” Invest. Ophthalmol. Visual Sci.
, 32
(8
), pp. 2244
–2258
.53.
Haider
, M. A.
, and Guilak
, F.
, 2007, “Application of a Three-Dimensional Poroelastic BEM to Modeling the Biphasic Mechanics of Cell-Matrix Interactions in Articular Cartilage
,” Comput. Methods Applied Mech. Eng.
, 196
(31-32
), pp. 2999
–3010
.54.
Ma
, J.
, Narayanan
, H.
, Garikipati
, K.
, Grosh
, K.
, and Arruda
, E. M.
, 2010, “Experimental and Computational Investigation of Viscoelasticity of Native and Engineered Ligament and Tendon
,” Proc. IUTAM Symposium on Cellular, Molecular and Tissue Mechanics
, Vol. 16
, pp. 3
–17
.55.
Greene
, P. R.
, 1980, “Mechanical Considerations in Myopia - Relative Effects of Accommodation, Convergence, Intraocular-Pressure, and the Extra-Ocular Muscles
,” Am. J. Optom. Physiol. Opt.
, 57
(12
), pp. 902
–914
.56.
Chen
, X. C.
, Zohdy
, M. J.
, Emelianov
, S. Y.
, and O’Donnell
, M.
, 2004, “Lateral Speckle Tracking Using Synthetic Lateral Phase
,” IEEEeee Trans. Ultrason. Ferroelectr. Freq. Control
, 51
(5
), pp. 540
–550
.57.
Huang
, Y.
, and Meek
, K. M.
, 1999, “Swelling Studies on the Cornea and Sclera: The Effects of pH and Ionic Strength
,” Biophys. J.
, 77
(3
), pp. 1655
–1665
.Copyright © 2012
by American Society of Mechanical Engineers
You do not currently have access to this content.
