Quantitative Assessment of Thin-Layer Tissue Viscoelastic Properties Using Ultrasonic Micro-Elastography With Lamb Wave Model

Characterizing the viscoelastic properties of thin-layer tissues with micro-level thickness has long remained challenging. Recently, several micro-elastography techniques have been developed to improve the spatial resolution. However, most of these techniques have not considered the medium boundary conditions when evaluating the viscoelastic properties of thin-layer tissues such as arteries and corneas; this might lead to estimation bias or errors. This paper aims to integrate the Lamb wave model with our previously developed ultrasonic micro-elastography imaging system for obtaining accurate viscoelastic properties in thin-layer tissues. A 4.5-MHz ring transducer was used to generate an acoustic radiation force for inducing tissue displacements to produce guided wave, and the wave propagation was detected using a confocally aligned 40-MHz needle transducer. The phase velocity and attenuation were obtained from k-space by both the impulse and the harmonic methods. The measured phase velocity was fit using the Lamb wave model with the Kelvin–Voigt model. Phantom experiments were conducted using 7% and 12% gelatin and 1.5% agar phantoms with different thicknesses (2, 3, and 4 mm). Biological experiments were performed on porcine cornea and rabbit carotid artery <italic>ex vivo</italic>. Thin-layer phantoms with different thicknesses were confirmed to have the same elasticity; this was consistent with the estimates of bulk phantoms from mechanical tests and the shear wave rheological model. The trend of the measured attenuations was also confirmed with the viscosity results obtained using the Lamb wave model. Through the impulse and harmonic methods, the shear viscoelasticity values were estimated to be 8.2 kPa for <inline-formula> <tex-math notation="LaTeX">$0.9~\text {Pa}{\cdot} \text {s}$ </tex-math></inline-formula> and 9.6 kPa for <inline-formula> <tex-math notation="LaTeX">$0.8~\text {Pa}{\cdot} \text {s}$ </tex-math></inline-formula> in the cornea and 27.9 kPa for <inline-formula> <tex-math notation="LaTeX">$0.1~\text {Pa}\cdot \text {s}$ </tex-math></inline-formula> and 26.5 kPa for <inline-formula> <tex-math notation="LaTeX">$0.1~\text {Pa}\cdot \text {s}$ </tex-math></inline-formula> in the artery.

[1]  J. Cohn,et al.  Arterial stiffness as a risk factor for coronary atherosclerosis , 2007, Current atherosclerosis reports.

[2]  Choon-Sik Jhun,et al.  Comparison of porcine pulmonary and aortic root material properties. , 2010, The Annals of thoracic surgery.

[3]  Caitriona Kirwan,et al.  Corneal hysteresis using the Reichert ocular response analyser: findings pre‐ and post‐LASIK and LASEK , 2008, Acta ophthalmologica.

[4]  M Fink,et al.  Measurement of viscoelastic properties of homogeneous soft solid using transient elastography: An inverse problem approach , 2004 .

[5]  R. Panerai,et al.  Shear wave elastography assessment of carotid plaque stiffness: in vitro reproducibility study. , 2014, Ultrasound in medicine & biology.

[6]  Matthew W Urban,et al.  Lamb wave dispersion ultrasound vibrometry (LDUV) method for quantifying mechanical properties of viscoelastic solids , 2011, Physics in medicine and biology.

[7]  Zhongping Chen,et al.  Resonant acoustic radiation force optical coherence elastography. , 2013, Applied physics letters.

[8]  Nathan M. Radcliffe,et al.  Corneal hysteresis and its relevance to glaucoma , 2015, Current opinion in ophthalmology.

[9]  Chih-Chung Huang,et al.  Estimating the viscoelastic modulus of a thrombus using an ultrasonic shear-wave approach. , 2013, Medical physics.

[10]  R L Ehman,et al.  Vascular wall elasticity measurement by magnetic resonance imaging , 2006, Magnetic resonance in medicine.

[11]  J. Carroll,et al.  Determination of pulse wave velocities with computerized algorithms. , 1991, American heart journal.

[12]  David Saloner,et al.  Significant material property differences between the porcine ascending aorta and aortic sinuses. , 2008, The Journal of heart valve disease.

[13]  Knut Brabrand,et al.  Assessment of renal allograft fibrosis by acoustic radiation force impulse quantification – a pilot study , 2011, Transplant international : official journal of the European Society for Organ Transplantation.

[14]  E. Konofagou,et al.  Pulse wave imaging for noninvasive and quantitative measurement of arterial stiffness in vivo. , 2010, American journal of hypertension.

[15]  M. Fatemi,et al.  Noninvasive method for estimation of complex elastic modulus of arterial vessels , 2005, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[16]  Ghassan S Kassab,et al.  Right coronary artery becomes stiffer with increase in elastin and collagen in right ventricular hypertrophy. , 2009, Journal of applied physiology.

[17]  M. Tanter,et al.  Assessment of viscous and elastic properties of sub-wavelength layered soft tissues using shear wave spectroscopy: Theoretical framework and in vitro experimental validation , 2011, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[18]  Chih-Chung Huang,et al.  Assessing the viscoelastic properties of thrombus using a solid-sphere-based instantaneous force approach. , 2011, Ultrasound in medicine & biology.

[19]  S. Laurent,et al.  Aortic Stiffness Is an Independent Predictor of Fatal Stroke in Essential Hypertension , 2003, Stroke.

[20]  Matthew O'Donnell,et al.  Strain Imaging of Corneal Tissue With an Ultrasound Elasticity Microscope , 2002, Cornea.

[21]  Kathryn R Nightingale,et al.  Accounting for the Spatial Observation Window in the 2-D Fourier Transform Analysis of Shear Wave Attenuation. , 2017, Ultrasound in medicine & biology.

[22]  Matthew W Urban,et al.  Acoustic waves in medical imaging and diagnostics. , 2013, Ultrasound in medicine & biology.

[23]  Ruikang K. Wang,et al.  Acoustic micro-tapping for non-contact 4D imaging of tissue elasticity , 2016, Scientific Reports.

[24]  K. Larin,et al.  Quantitative methods for reconstructing tissue biomechanical properties in optical coherence elastography: a comparison study , 2015, Physics in medicine and biology.

[25]  Qifa Zhou,et al.  Acoustic Radiation Force Optical Coherence Elastography of Corneal Tissue , 2016, IEEE Journal of Selected Topics in Quantum Electronics.

[26]  M. Fink,et al.  Quantitative assessment of arterial wall biomechanical properties using shear wave imaging. , 2010, Ultrasound in medicine & biology.

[27]  Shigao Chen,et al.  Shearwave dispersion ultrasound vibrometry (SDUV) for measuring tissue elasticity and viscosity , 2009, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[28]  Matthew W Urban,et al.  Phase velocities and attenuations of shear, Lamb, and Rayleigh waves in plate-like tissues submerged in a fluid (L). , 2011, The Journal of the Acoustical Society of America.

[29]  Chih-Chung Huang,et al.  Evaluating the intensity of the acoustic radiation force impulse (ARFI) in intravascular ultrasound (IVUS) imaging: Preliminary in vitro results. , 2016, Ultrasonics.

[30]  M Alevizaki,et al.  Arterial stiffness in Type 1 diabetes mellitus is aggravated by autoimmune thyroid disease , 2005, Journal of endocrinological investigation.

[31]  K. Nightingale,et al.  Quantifying hepatic shear modulus in vivo using acoustic radiation force. , 2008, Ultrasound in medicine & biology.

[32]  Mostafa Fatemi,et al.  Quantifying elasticity and viscosity from measurement of shear wave speed dispersion. , 2004, The Journal of the Acoustical Society of America.

[33]  K. Larin,et al.  Optical coherence elastography assessment of corneal viscoelasticity with a modified Rayleigh-Lamb wave model. , 2017, Journal of the mechanical behavior of biomedical materials.

[34]  Hiroshi Kanai,et al.  Measurement of shear wave propagation and investigation of estimation of shear viscoelasticity for tissue characterization of the arterial wall , 2005, Journal of Medical Ultrasonics.

[35]  C. Vlachopoulos,et al.  Prediction of Cardiovascular Events and All-Cause Mortality With Arterial Stiffness , 2011 .

[36]  M L Bots,et al.  Common carotid intima-media thickness and arterial stiffness: indicators of cardiovascular risk in high-risk patients. The SMART Study (Second Manifestations of ARTerial disease). , 1999, Circulation.

[37]  Thomas Deffieux,et al.  Quantitative assessment of breast lesion viscoelasticity: initial clinical results using supersonic shear imaging. , 2008, Ultrasound in medicine & biology.

[38]  S. Emelianov,et al.  Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics. , 1998, Ultrasound in medicine & biology.

[39]  K V Ramnarine,et al.  Shear Wave Elastography May Be Superior to Greyscale Median for the Identification of Carotid Plaque Vulnerability: A Comparison with Histology , 2015, Ultraschall in der Medizin.

[40]  J. Greenleaf,et al.  Material property estimation for tubes and arteries using ultrasound radiation force and analysis of propagating modes. , 2011, The Journal of the Acoustical Society of America.

[41]  Matilda Larsson,et al.  Influence of wall thickness and diameter on arterial shear wave elastography: a phantom and finite element study , 2017, Physics in medicine and biology.

[42]  Ned C. Rouze,et al.  Dependence of shear wave spectral content on acoustic radiation force excitation duration and spatial beamwidth , 2014, 2014 IEEE International Ultrasonics Symposium.

[43]  Matthew W Urban,et al.  On Lamb and Rayleigh wave convergence in viscoelastic tissues , 2011, Physics in medicine and biology.

[44]  Ghassan S Kassab,et al.  A rate-insensitive linear viscoelastic model for soft tissues. , 2007, Biomaterials.

[45]  K. Larin,et al.  Analysis of the effects of curvature and thickness on elastic wave velocity in cornea-like structures by finite element modeling and optical coherence elastography. , 2015, Applied physics letters.

[46]  Nathan D. Shemonski,et al.  Magnetomotive optical coherence elastography using magnetic particles to induce mechanical waves. , 2014, Biomedical optics express.

[47]  David Larsson,et al.  Arterial Stiffness Estimation by Shear Wave Elastography: Validation in Phantoms with Mechanical Testing. , 2016, Ultrasound in medicine & biology.

[48]  C. D. A. Stehouwer,et al.  Arterial stiffness in diabetes and the metabolic syndrome: a pathway to cardiovascular disease , 2008, Diabetologia.

[49]  Qifa Zhou,et al.  High-Resolution Acoustic-Radiation-Force-Impulse Imaging for Assessing Corneal Sclerosis , 2013, IEEE Transactions on Medical Imaging.

[50]  G. Trahey,et al.  Shear-wave generation using acoustic radiation force: in vivo and ex vivo results. , 2003, Ultrasound in medicine & biology.

[51]  S. Emelianov,et al.  Assessment of shear modulus of tissue using ultrasound radiation force acting on a spherical acoustic inhomogeneity , 2009, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[52]  Pai-Chi Li,et al.  Shear-wave elasticity measurements of three-dimensional cell cultures for mechanobiology , 2017, Journal of Cell Science.

[53]  Qifa Zhou,et al.  Multi-functional Ultrasonic Micro-elastography Imaging System , 2017, Scientific Reports.

[54]  D. Luce Determining in vivo biomechanical properties of the cornea with an ocular response analyzer , 2005, Journal of cataract and refractive surgery.

[55]  Bo Qiang,et al.  Attenuation measuring ultrasound shearwave elastography and in vivo application in post-transplant liver patients , 2017, Physics in medicine and biology.

[56]  D. Sampson,et al.  Spectroscopic optical coherence elastography , 2010, Optics express.

[57]  Qifa Zhou,et al.  High-resolution harmonic motion imaging (HR-HMI) for tissue biomechanical property characterization. , 2015, Quantitative imaging in medicine and surgery.

[58]  Matilda Larsson,et al.  Shear Wave Elastography Quantifies Stiffness in Ex Vivo Porcine Artery with Stiffened Arterial Region. , 2016, Ultrasound in medicine & biology.

[59]  K. Larin,et al.  Shear wave imaging optical coherence tomography (SWI-OCT) for ocular tissue biomechanics. , 2014, Optics letters.

[60]  Mathias Fink,et al.  High-Resolution Quantitative Imaging of Cornea Elasticity Using Supersonic Shear Imaging , 2009, IEEE Transactions on Medical Imaging.