Abstract

We report on a quantitative optical elastographic method based on shear wave imaging optical coherence tomography (SWI-OCT) for biomechanical characterization of cardiac muscle through noncontact elasticity measurement. The SWI-OCT system employs a focused air-puff device for localized loading of the cardiac muscle and utilizes phase-sensitive OCT to monitor the induced tissue deformation. Phase information from the optical interferometry is used to reconstruct 2-D depth-resolved shear wave propagation inside the muscle tissue. Cross-correlation of the displacement profiles at various spatial locations in the propagation direction is applied to measure the group velocity of the shear waves, based on which the Young’s modulus of tissue is quantified. The quantitative feature and measurement accuracy of this method is demonstrated from the experiments on tissue-mimicking phantoms with the verification using uniaxial compression test. The experiments are performed on ex vivo cardiac muscle tissue from mice with normal and genetically altered myocardium. Our results indicate this optical elastographic technique is useful as a noncontact tool to assist the cardiac muscle studies.

© 2014 Optical Society of America

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2014 (6)

B. F. Kennedy, K. M. Kennedy, and D. D. Sampson, “A Review of Optical Coherence Elastography: Fundamentals, Techniques and Prospects,” IEEE J. Sel. Top. Quantum Electron.20(2), 1–17 (2014).
[CrossRef]

T. M. Nguyen, S. Song, B. Arnal, E. Y. Wong, Z. Huang, R. K. Wang, and M. O’Donnell, “Shear wave pulse compression for dynamic elastography using phase-sensitive optical coherence tomography,” J. Biomed. Opt.19(1), 016013 (2014).
[CrossRef] [PubMed]

S. Wang and K. V. Larin, “Shear wave imaging optical coherence tomography (SWI-OCT) for ocular tissue biomechanics,” Opt. Lett.39(1), 41–44 (2014).
[CrossRef] [PubMed]

T.-M. Nguyen, S. Song, B. Arnal, Z. Huang, M. O’Donnell, and R. K. Wang, “Visualizing ultrasonically induced shear wave propagation using phase-sensitive optical coherence tomography for dynamic elastography,” Opt. Lett.39(4), 838–841 (2014).
[CrossRef] [PubMed]

M. Razani, T. W. H. Luk, A. Mariampillai, P. Siegler, T.-R. Kiehl, M. C. Kolios, and V. X. D. Yang, “Optical coherence tomography detection of shear wave propagation in inhomogeneous tissue equivalent phantoms and ex-vivo carotid artery samples,” Biomed. Opt. Express5(3), 895–906 (2014).
[CrossRef] [PubMed]

B. R. Klyen, L. Scolaro, T. Shavlakadze, M. D. Grounds, and D. D. Sampson, “Optical coherence tomography can assess skeletal muscle tissue from mouse models of muscular dystrophy by parametric imaging of the attenuation coefficient,” Biomed. Opt. Express5(4), 1217–1232 (2014).
[CrossRef] [PubMed]

2013 (11)

C. Fan and G. Yao, “Imaging myocardial fiber orientation using polarization sensitive optical coherence tomography,” Biomed. Opt. Express4(3), 460–465 (2013).
[CrossRef] [PubMed]

M. W. Jenkins, Y. T. Wang, Y. Q. Doughman, M. Watanabe, Y. Cheng, and A. M. Rollins, “Optical pacing of the adult rabbit heart,” Biomed. Opt. Express4(9), 1626–1635 (2013).
[CrossRef] [PubMed]

A. Nahas, M. Bauer, S. Roux, and A. C. Boccara, “3D static elastography at the micrometer scale using Full Field OCT,” Biomed. Opt. Express4(10), 2138–2149 (2013).
[CrossRef] [PubMed]

S. Song, Z. Huang, T. M. Nguyen, E. Y. Wong, B. Arnal, M. O’Donnell, and R. K. Wang, “Shear modulus imaging by direct visualization of propagating shear waves with phase-sensitive optical coherence tomography,” J. Biomed. Opt.18(12), 121509 (2013).
[CrossRef] [PubMed]

K. M. Kennedy, C. Ford, B. F. Kennedy, M. B. Bush, and D. D. Sampson, “Analysis of mechanical contrast in optical coherence elastography,” J. Biomed. Opt.18(12), 121508 (2013).
[CrossRef] [PubMed]

T. Heallen, Y. Morikawa, J. Leach, G. Tao, J. T. Willerson, R. L. Johnson, and J. F. Martin, “Hippo signaling impedes adult heart regeneration,” Development140(23), 4683–4690 (2013).
[CrossRef] [PubMed]

M. Xin, Y. Kim, L. B. Sutherland, M. Murakami, X. Qi, J. McAnally, E. R. Porrello, A. I. Mahmoud, W. Tan, J. M. Shelton, J. A. Richardson, H. A. Sadek, R. Bassel-Duby, and E. N. Olson, “Hippo pathway effector Yap promotes cardiac regeneration,” Proc. Natl. Acad. Sci. U.S.A.110(34), 13839–13844 (2013).
[CrossRef] [PubMed]

S. L. Murphy, J. Xu, and K. D. Kochanek, “Deaths: Final Data for 2010,” Natl. Vital Stat. Rep.61, 1–117 (2013).

V. Crecea, A. Ahmad, and S. A. Boppart, “Magnetomotive optical coherence elastography for microrheology of biological tissues,” J. Biomed. Opt.18(12), 121504 (2013).
[CrossRef] [PubMed]

S. Wang, K. V. Larin, J. Li, S. Vantipalli, R. K. Manapuram, S. Aglyamov, S. Emelianov, and M. D. Twa, “A focused air-pulse system for optical-coherence-tomography-based measurements of tissue elasticity,” Laser Phys. Lett.10(7), 075605 (2013).
[CrossRef]

S. Song, Z. Huang, and R. K. Wang, “Tracking mechanical wave propagation within tissue using phase-sensitive optical coherence tomography: motion artifact and its compensation,” J. Biomed. Opt.18(12), 121505 (2013).
[CrossRef] [PubMed]

2012 (9)

W. Qi, R. Chen, L. Chou, G. Liu, J. Zhang, Q. Zhou, and Z. Chen, “Phase-resolved acoustic radiation force optical coherence elastography,” J. Biomed. Opt.17(11), 110505 (2012).
[CrossRef] [PubMed]

W. Hiesinger, M. J. Brukman, R. C. McCormick, J. R. Fitzpatrick, J. R. Frederick, E. C. Yang, J. R. Muenzer, N. A. Marotta, M. F. Berry, P. Atluri, and Y. J. Woo, “Myocardial tissue elastic properties determined by atomic force microscopy after stromal cell-derived factor 1α angiogenic therapy for acute myocardial infarction in a murine model,” J. Thorac. Cardiovasc. Surg.143(4), 962–966 (2012).
[CrossRef] [PubMed]

C. Li, G. Guan, R. Reif, Z. Huang, and R. K. Wang, “Determining elastic properties of skin by measuring surface waves from an impulse mechanical stimulus using phase-sensitive optical coherence tomography,” J. R. Soc. Interface9(70), 831–841 (2012).
[CrossRef] [PubMed]

C. Li, G. Guan, X. Cheng, Z. Huang, and R. K. Wang, “Quantitative elastography provided by surface acoustic waves measured by phase-sensitive optical coherence tomography,” Opt. Lett.37(4), 722–724 (2012).
[CrossRef] [PubMed]

I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Sequential Turning Acquisition and Reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures,” Biomed. Opt. Express3(3), 650–660 (2012).
[CrossRef] [PubMed]

M. Razani, A. Mariampillai, C. Sun, T. W. H. Luk, V. X. D. Yang, and M. C. Kolios, “Feasibility of optical coherence elastography measurements of shear wave propagation in homogeneous tissue equivalent phantoms,” Biomed. Opt. Express3(5), 972–980 (2012).
[CrossRef] [PubMed]

C. Li, G. Guan, Z. Huang, M. Johnstone, and R. K. Wang, “Noncontact all-optical measurement of corneal elasticity,” Opt. Lett.37(10), 1625–1627 (2012).
[CrossRef] [PubMed]

K. M. Kennedy, B. F. Kennedy, R. A. McLaughlin, and D. D. Sampson, “Needle optical coherence elastography for tissue boundary detection,” Opt. Lett.37(12), 2310–2312 (2012).
[CrossRef] [PubMed]

S. Wang, J. Li, R. K. Manapuram, F. M. Menodiado, D. R. Ingram, M. D. Twa, A. J. Lazar, D. C. Lev, R. E. Pollock, and K. V. Larin, “Noncontact measurement of elasticity for the detection of soft-tissue tumors using phase-sensitive optical coherence tomography combined with a focused air-puff system,” Opt. Lett.37(24), 5184–5186 (2012).
[CrossRef] [PubMed]

2011 (7)

C. Sun, B. Standish, and V. X. D. Yang, “Optical coherence elastography: current status and future applications,” J. Biomed. Opt.16(4), 043001 (2011).
[CrossRef] [PubMed]

M. Mercola, P. Ruiz-Lozano, and M. D. Schneider, “Cardiac muscle regeneration: lessons from development,” Genes Dev.25(4), 299–309 (2011).
[CrossRef] [PubMed]

P. N. Wells and H. D. Liang, “Medical ultrasound: imaging of soft tissue strain and elasticity,” J. R. Soc. Interface8(64), 1521–1549 (2011).
[CrossRef] [PubMed]

A. Biernacka and N. G. Frangogiannis, “Aging and Cardiac Fibrosis,” Aging Dis.2(2), 158–173 (2011).
[PubMed]

B. F. Kennedy, X. Liang, S. G. Adie, D. K. Gerstmann, B. C. Quirk, S. A. Boppart, and D. D. Sampson, “In vivo three-dimensional optical coherence elastography,” Opt. Express19(7), 6623–6634 (2011).
[CrossRef] [PubMed]

C. Li, Z. Huang, and R. K. Wang, “Elastic properties of soft tissue-mimicking phantoms assessed by combined use of laser ultrasonics and low coherence interferometry,” Opt. Express19(11), 10153–10163 (2011).
[CrossRef] [PubMed]

L. An, P. Li, T. T. Shen, and R. Wang, “High speed spectral domain optical coherence tomography for retinal imaging at 500,000 A‑lines per second,” Biomed. Opt. Express2(10), 2770–2783 (2011).
[CrossRef] [PubMed]

2010 (6)

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]

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]

A. L. Oldenburg and S. A. Boppart, “Resonant acoustic spectroscopy of soft tissues using embedded magnetomotive nanotransducers and optical coherence tomography,” Phys. Med. Biol.55(4), 1189–1201 (2010).
[CrossRef] [PubMed]

Y. K. Mariappan, K. J. Glaser, and R. L. Ehman, “Magnetic resonance elastography: a review,” Clin. Anat.23(5), 497–511 (2010).
[CrossRef] [PubMed]

X. Liang, V. Crecea, and S. A. Boppart, “Dynamic optical coherence elastography: a review,” J. Innov. Opt. Health Sci.3(4), 221–233 (2010).
[CrossRef] [PubMed]

X. Liang and S. A. Boppart, “Biomechanical properties of In vivo human skin from dynamic optical coherence elastography,” IEEE Trans. Biomed. Eng.57(4), 953–959 (2010).
[CrossRef] [PubMed]

2009 (3)

S. G. Adie, B. F. Kennedy, J. J. Armstrong, S. A. Alexandrov, and D. D. Sampson, “Audio frequency in vivo optical coherence elastography,” Phys. Med. Biol.54(10), 3129–3139 (2009).
[CrossRef] [PubMed]

S. Chen, M. W. Urban, C. Pislaru, R. Kinnick, Y. Zheng, A. Yao, and J. F. Greenleaf, “Shearwave dispersion ultrasound vibrometry (SDUV) for measuring tissue elasticity and viscosity,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control56(1), 55–62 (2009).
[CrossRef] [PubMed]

B. F. Kennedy, T. R. Hillman, R. A. McLaughlin, B. C. Quirk, and D. D. Sampson, “In vivo dynamic optical coherence elastography using a ring actuator,” Opt. Express17(24), 21762–21772 (2009).
[CrossRef] [PubMed]

2008 (2)

2007 (2)

R. M. Setser, N. G. Smedira, M. L. Lieber, E. D. Sabo, and R. D. White, “Left ventricular torsional mechanics after left ventricular reconstruction surgery for ischemic cardiomyopathy,” J. Thorac. Cardiovasc. Surg.134(4), 888–896 (2007).
[CrossRef] [PubMed]

T. G. Kuznetsova, M. N. Starodubtseva, N. I. Yegorenkov, S. A. Chizhik, and R. I. Zhdanov, “Atomic force microscopy probing of cell elasticity,” Micron38(8), 824–833 (2007).
[CrossRef] [PubMed]

2005 (2)

M. A. Choma, A. K. Ellerbee, C. Yang, T. L. Creazzo, and J. A. Izatt, “Spectral-domain phase microscopy,” Opt. Lett.30(10), 1162–1164 (2005).
[CrossRef] [PubMed]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt.10(5), 054001 (2005).
[CrossRef] [PubMed]

2004 (1)

J. Bercoff, M. Tanter, and M. Fink, “Supersonic shear imaging: a new technique for soft tissue elasticity mapping,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(4), 396–409 (2004).
[CrossRef] [PubMed]

2001 (1)

A. B. Mathur, A. M. Collinsworth, W. M. Reichert, W. E. Kraus, and G. A. Truskey, “Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy,” J. Biomech.34(12), 1545–1553 (2001).
[CrossRef] [PubMed]

1999 (1)

J. Xia, R. D. Miller, and C. B. Park, “Estimation of near-surface shear-wave velocity by inversion of Rayleigh waves,” Geophysics64(3), 691–700 (1999).
[CrossRef]

1998 (2)

J. Schmitt, “OCT elastography: imaging microscopic deformation and strain of tissue,” Opt. Express3(6), 199–211 (1998).
[CrossRef] [PubMed]

A. P. Sarvazyan, O. V. Rudenko, S. D. Swanson, J. B. Fowlkes, and S. Y. Emelianov, “Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics,” Ultrasound Med. Biol.24(9), 1419–1435 (1998).
[CrossRef] [PubMed]

1981 (1)

R. C. Chivers, “Tissue characterization,” Ultrasound Med. Biol.7(1), 1–20 (1981).
[CrossRef] [PubMed]

1955 (1)

D. G. Melrose, B. Dreyer, H. H. Bentall, and J. B. E. Baker, “Elective Cardiac Arrest,” Lancet266(6879), 21–23 (1955).
[CrossRef] [PubMed]

Adie, S. G.

Aglyamov, S.

S. Wang, K. V. Larin, J. Li, S. Vantipalli, R. K. Manapuram, S. Aglyamov, S. Emelianov, and M. D. Twa, “A focused air-pulse system for optical-coherence-tomography-based measurements of tissue elasticity,” Laser Phys. Lett.10(7), 075605 (2013).
[CrossRef]

Ahmad, A.

V. Crecea, A. Ahmad, and S. A. Boppart, “Magnetomotive optical coherence elastography for microrheology of biological tissues,” J. Biomed. Opt.18(12), 121504 (2013).
[CrossRef] [PubMed]

Alexandrov, S. A.

S. G. Adie, B. F. Kennedy, J. J. Armstrong, S. A. Alexandrov, and D. D. Sampson, “Audio frequency in vivo optical coherence elastography,” Phys. Med. Biol.54(10), 3129–3139 (2009).
[CrossRef] [PubMed]

Ali, N. N.

H. Jawad, A. R. Lyon, S. E. Harding, N. N. Ali, and A. R. Boccaccini, “Myocardial tissue engineering,” Br. Med. Bull.87(1), 31–47 (2008).
[CrossRef] [PubMed]

An, L.

Armstrong, J. J.

S. G. Adie, B. F. Kennedy, J. J. Armstrong, S. A. Alexandrov, and D. D. Sampson, “Audio frequency in vivo optical coherence elastography,” Phys. Med. Biol.54(10), 3129–3139 (2009).
[CrossRef] [PubMed]

Arnal, B.

T. M. Nguyen, S. Song, B. Arnal, E. Y. Wong, Z. Huang, R. K. Wang, and M. O’Donnell, “Shear wave pulse compression for dynamic elastography using phase-sensitive optical coherence tomography,” J. Biomed. Opt.19(1), 016013 (2014).
[CrossRef] [PubMed]

T.-M. Nguyen, S. Song, B. Arnal, Z. Huang, M. O’Donnell, and R. K. Wang, “Visualizing ultrasonically induced shear wave propagation using phase-sensitive optical coherence tomography for dynamic elastography,” Opt. Lett.39(4), 838–841 (2014).
[CrossRef] [PubMed]

S. Song, Z. Huang, T. M. Nguyen, E. Y. Wong, B. Arnal, M. O’Donnell, and R. K. Wang, “Shear modulus imaging by direct visualization of propagating shear waves with phase-sensitive optical coherence tomography,” J. Biomed. Opt.18(12), 121509 (2013).
[CrossRef] [PubMed]

Atluri, P.

W. Hiesinger, M. J. Brukman, R. C. McCormick, J. R. Fitzpatrick, J. R. Frederick, E. C. Yang, J. R. Muenzer, N. A. Marotta, M. F. Berry, P. Atluri, and Y. J. Woo, “Myocardial tissue elastic properties determined by atomic force microscopy after stromal cell-derived factor 1α angiogenic therapy for acute myocardial infarction in a murine model,” J. Thorac. Cardiovasc. Surg.143(4), 962–966 (2012).
[CrossRef] [PubMed]

Baker, J. B. E.

D. G. Melrose, B. Dreyer, H. H. Bentall, and J. B. E. Baker, “Elective Cardiac Arrest,” Lancet266(6879), 21–23 (1955).
[CrossRef] [PubMed]

Bassel-Duby, R.

M. Xin, Y. Kim, L. B. Sutherland, M. Murakami, X. Qi, J. McAnally, E. R. Porrello, A. I. Mahmoud, W. Tan, J. M. Shelton, J. A. Richardson, H. A. Sadek, R. Bassel-Duby, and E. N. Olson, “Hippo pathway effector Yap promotes cardiac regeneration,” Proc. Natl. Acad. Sci. U.S.A.110(34), 13839–13844 (2013).
[CrossRef] [PubMed]

Bauer, M.

Bentall, H. H.

D. G. Melrose, B. Dreyer, H. H. Bentall, and J. B. E. Baker, “Elective Cardiac Arrest,” Lancet266(6879), 21–23 (1955).
[CrossRef] [PubMed]

Bercoff, J.

J. Bercoff, M. Tanter, and M. Fink, “Supersonic shear imaging: a new technique for soft tissue elasticity mapping,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(4), 396–409 (2004).
[CrossRef] [PubMed]

Berry, M. F.

W. Hiesinger, M. J. Brukman, R. C. McCormick, J. R. Fitzpatrick, J. R. Frederick, E. C. Yang, J. R. Muenzer, N. A. Marotta, M. F. Berry, P. Atluri, and Y. J. Woo, “Myocardial tissue elastic properties determined by atomic force microscopy after stromal cell-derived factor 1α angiogenic therapy for acute myocardial infarction in a murine model,” J. Thorac. Cardiovasc. Surg.143(4), 962–966 (2012).
[CrossRef] [PubMed]

Biernacka, A.

A. Biernacka and N. G. Frangogiannis, “Aging and Cardiac Fibrosis,” Aging Dis.2(2), 158–173 (2011).
[PubMed]

Boccaccini, A. R.

H. Jawad, A. R. Lyon, S. E. Harding, N. N. Ali, and A. R. Boccaccini, “Myocardial tissue engineering,” Br. Med. Bull.87(1), 31–47 (2008).
[CrossRef] [PubMed]

Boccara, A. C.

Boppart, S. A.

V. Crecea, A. Ahmad, and S. A. Boppart, “Magnetomotive optical coherence elastography for microrheology of biological tissues,” J. Biomed. Opt.18(12), 121504 (2013).
[CrossRef] [PubMed]

B. F. Kennedy, X. Liang, S. G. Adie, D. K. Gerstmann, B. C. Quirk, S. A. Boppart, and D. D. Sampson, “In vivo three-dimensional optical coherence elastography,” Opt. Express19(7), 6623–6634 (2011).
[CrossRef] [PubMed]

X. Liang, V. Crecea, and S. A. Boppart, “Dynamic optical coherence elastography: a review,” J. Innov. Opt. Health Sci.3(4), 221–233 (2010).
[CrossRef] [PubMed]

X. Liang and S. A. Boppart, “Biomechanical properties of In vivo human skin from dynamic optical coherence elastography,” IEEE Trans. Biomed. Eng.57(4), 953–959 (2010).
[CrossRef] [PubMed]

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]

A. L. Oldenburg and S. A. Boppart, “Resonant acoustic spectroscopy of soft tissues using embedded magnetomotive nanotransducers and optical coherence tomography,” Phys. Med. Biol.55(4), 1189–1201 (2010).
[CrossRef] [PubMed]

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]

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]

Brukman, M. J.

W. Hiesinger, M. J. Brukman, R. C. McCormick, J. R. Fitzpatrick, J. R. Frederick, E. C. Yang, J. R. Muenzer, N. A. Marotta, M. F. Berry, P. Atluri, and Y. J. Woo, “Myocardial tissue elastic properties determined by atomic force microscopy after stromal cell-derived factor 1α angiogenic therapy for acute myocardial infarction in a murine model,” J. Thorac. Cardiovasc. Surg.143(4), 962–966 (2012).
[CrossRef] [PubMed]

Bush, M. B.

K. M. Kennedy, C. Ford, B. F. Kennedy, M. B. Bush, and D. D. Sampson, “Analysis of mechanical contrast in optical coherence elastography,” J. Biomed. Opt.18(12), 121508 (2013).
[CrossRef] [PubMed]

Chaney, E. J.

Chen, R.

W. Qi, R. Chen, L. Chou, G. Liu, J. Zhang, Q. Zhou, and Z. Chen, “Phase-resolved acoustic radiation force optical coherence elastography,” J. Biomed. Opt.17(11), 110505 (2012).
[CrossRef] [PubMed]

Chen, S.

S. Chen, M. W. Urban, C. Pislaru, R. Kinnick, Y. Zheng, A. Yao, and J. F. Greenleaf, “Shearwave dispersion ultrasound vibrometry (SDUV) for measuring tissue elasticity and viscosity,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control56(1), 55–62 (2009).
[CrossRef] [PubMed]

Chen, Z.

W. Qi, R. Chen, L. Chou, G. Liu, J. Zhang, Q. Zhou, and Z. Chen, “Phase-resolved acoustic radiation force optical coherence elastography,” J. Biomed. Opt.17(11), 110505 (2012).
[CrossRef] [PubMed]

Cheng, X.

Cheng, Y.

Chivers, R. C.

R. C. Chivers, “Tissue characterization,” Ultrasound Med. Biol.7(1), 1–20 (1981).
[CrossRef] [PubMed]

Chizhik, S. A.

T. G. Kuznetsova, M. N. Starodubtseva, N. I. Yegorenkov, S. A. Chizhik, and R. I. Zhdanov, “Atomic force microscopy probing of cell elasticity,” Micron38(8), 824–833 (2007).
[CrossRef] [PubMed]

Choma, M. A.

Chou, L.

W. Qi, R. Chen, L. Chou, G. Liu, J. Zhang, Q. Zhou, and Z. Chen, “Phase-resolved acoustic radiation force optical coherence elastography,” J. Biomed. Opt.17(11), 110505 (2012).
[CrossRef] [PubMed]

Collinsworth, A. M.

A. B. Mathur, A. M. Collinsworth, W. M. Reichert, W. E. Kraus, and G. A. Truskey, “Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy,” J. Biomech.34(12), 1545–1553 (2001).
[CrossRef] [PubMed]

Creazzo, T. L.

Crecea, V.

V. Crecea, A. Ahmad, and S. A. Boppart, “Magnetomotive optical coherence elastography for microrheology of biological tissues,” J. Biomed. Opt.18(12), 121504 (2013).
[CrossRef] [PubMed]

X. Liang, V. Crecea, and S. A. Boppart, “Dynamic optical coherence elastography: a review,” J. Innov. Opt. Health Sci.3(4), 221–233 (2010).
[CrossRef] [PubMed]

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]

Dickinson, M. E.

I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Sequential Turning Acquisition and Reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures,” Biomed. Opt. Express3(3), 650–660 (2012).
[CrossRef] [PubMed]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt.10(5), 054001 (2005).
[CrossRef] [PubMed]

Doughman, Y. Q.

Dreyer, B.

D. G. Melrose, B. Dreyer, H. H. Bentall, and J. B. E. Baker, “Elective Cardiac Arrest,” Lancet266(6879), 21–23 (1955).
[CrossRef] [PubMed]

Ehman, R. L.

Y. K. Mariappan, K. J. Glaser, and R. L. Ehman, “Magnetic resonance elastography: a review,” Clin. Anat.23(5), 497–511 (2010).
[CrossRef] [PubMed]

Ellerbee, A. K.

Emelianov, S.

S. Wang, K. V. Larin, J. Li, S. Vantipalli, R. K. Manapuram, S. Aglyamov, S. Emelianov, and M. D. Twa, “A focused air-pulse system for optical-coherence-tomography-based measurements of tissue elasticity,” Laser Phys. Lett.10(7), 075605 (2013).
[CrossRef]

Emelianov, S. Y.

A. P. Sarvazyan, O. V. Rudenko, S. D. Swanson, J. B. Fowlkes, and S. Y. Emelianov, “Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics,” Ultrasound Med. Biol.24(9), 1419–1435 (1998).
[CrossRef] [PubMed]

Fan, C.

Fink, M.

J. Bercoff, M. Tanter, and M. Fink, “Supersonic shear imaging: a new technique for soft tissue elasticity mapping,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control51(4), 396–409 (2004).
[CrossRef] [PubMed]

Fitzpatrick, J. R.

W. Hiesinger, M. J. Brukman, R. C. McCormick, J. R. Fitzpatrick, J. R. Frederick, E. C. Yang, J. R. Muenzer, N. A. Marotta, M. F. Berry, P. Atluri, and Y. J. Woo, “Myocardial tissue elastic properties determined by atomic force microscopy after stromal cell-derived factor 1α angiogenic therapy for acute myocardial infarction in a murine model,” J. Thorac. Cardiovasc. Surg.143(4), 962–966 (2012).
[CrossRef] [PubMed]

Ford, C.

K. M. Kennedy, C. Ford, B. F. Kennedy, M. B. Bush, and D. D. Sampson, “Analysis of mechanical contrast in optical coherence elastography,” J. Biomed. Opt.18(12), 121508 (2013).
[CrossRef] [PubMed]

Forouhar, A. S.

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt.10(5), 054001 (2005).
[CrossRef] [PubMed]

Fowlkes, J. B.

A. P. Sarvazyan, O. V. Rudenko, S. D. Swanson, J. B. Fowlkes, and S. Y. Emelianov, “Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics,” Ultrasound Med. Biol.24(9), 1419–1435 (1998).
[CrossRef] [PubMed]

Frangogiannis, N. G.

A. Biernacka and N. G. Frangogiannis, “Aging and Cardiac Fibrosis,” Aging Dis.2(2), 158–173 (2011).
[PubMed]

Fraser, S. E.

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt.10(5), 054001 (2005).
[CrossRef] [PubMed]

Frederick, J. R.

W. Hiesinger, M. J. Brukman, R. C. McCormick, J. R. Fitzpatrick, J. R. Frederick, E. C. Yang, J. R. Muenzer, N. A. Marotta, M. F. Berry, P. Atluri, and Y. J. Woo, “Myocardial tissue elastic properties determined by atomic force microscopy after stromal cell-derived factor 1α angiogenic therapy for acute myocardial infarction in a murine model,” J. Thorac. Cardiovasc. Surg.143(4), 962–966 (2012).
[CrossRef] [PubMed]

Gerstmann, D. K.

Gharib, M.

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt.10(5), 054001 (2005).
[CrossRef] [PubMed]

Glaser, K. J.

Y. K. Mariappan, K. J. Glaser, and R. L. Ehman, “Magnetic resonance elastography: a review,” Clin. Anat.23(5), 497–511 (2010).
[CrossRef] [PubMed]

Greenleaf, J. F.

S. Chen, M. W. Urban, C. Pislaru, R. Kinnick, Y. Zheng, A. Yao, and J. F. Greenleaf, “Shearwave dispersion ultrasound vibrometry (SDUV) for measuring tissue elasticity and viscosity,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control56(1), 55–62 (2009).
[CrossRef] [PubMed]

Grounds, M. D.

Guan, G.

Harding, S. E.

H. Jawad, A. R. Lyon, S. E. Harding, N. N. Ali, and A. R. Boccaccini, “Myocardial tissue engineering,” Br. Med. Bull.87(1), 31–47 (2008).
[CrossRef] [PubMed]

Heallen, T.

T. Heallen, Y. Morikawa, J. Leach, G. Tao, J. T. Willerson, R. L. Johnson, and J. F. Martin, “Hippo signaling impedes adult heart regeneration,” Development140(23), 4683–4690 (2013).
[CrossRef] [PubMed]

Hiesinger, W.

W. Hiesinger, M. J. Brukman, R. C. McCormick, J. R. Fitzpatrick, J. R. Frederick, E. C. Yang, J. R. Muenzer, N. A. Marotta, M. F. Berry, P. Atluri, and Y. J. Woo, “Myocardial tissue elastic properties determined by atomic force microscopy after stromal cell-derived factor 1α angiogenic therapy for acute myocardial infarction in a murine model,” J. Thorac. Cardiovasc. Surg.143(4), 962–966 (2012).
[CrossRef] [PubMed]

Hillman, T. R.

Huang, Z.

T.-M. Nguyen, S. Song, B. Arnal, Z. Huang, M. O’Donnell, and R. K. Wang, “Visualizing ultrasonically induced shear wave propagation using phase-sensitive optical coherence tomography for dynamic elastography,” Opt. Lett.39(4), 838–841 (2014).
[CrossRef] [PubMed]

T. M. Nguyen, S. Song, B. Arnal, E. Y. Wong, Z. Huang, R. K. Wang, and M. O’Donnell, “Shear wave pulse compression for dynamic elastography using phase-sensitive optical coherence tomography,” J. Biomed. Opt.19(1), 016013 (2014).
[CrossRef] [PubMed]

S. Song, Z. Huang, and R. K. Wang, “Tracking mechanical wave propagation within tissue using phase-sensitive optical coherence tomography: motion artifact and its compensation,” J. Biomed. Opt.18(12), 121505 (2013).
[CrossRef] [PubMed]

S. Song, Z. Huang, T. M. Nguyen, E. Y. Wong, B. Arnal, M. O’Donnell, and R. K. Wang, “Shear modulus imaging by direct visualization of propagating shear waves with phase-sensitive optical coherence tomography,” J. Biomed. Opt.18(12), 121509 (2013).
[CrossRef] [PubMed]

C. Li, G. Guan, R. Reif, Z. Huang, and R. K. Wang, “Determining elastic properties of skin by measuring surface waves from an impulse mechanical stimulus using phase-sensitive optical coherence tomography,” J. R. Soc. Interface9(70), 831–841 (2012).
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C. Li, G. Guan, X. Cheng, Z. Huang, and R. K. Wang, “Quantitative elastography provided by surface acoustic waves measured by phase-sensitive optical coherence tomography,” Opt. Lett.37(4), 722–724 (2012).
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C. Li, G. Guan, Z. Huang, M. Johnstone, and R. K. Wang, “Noncontact all-optical measurement of corneal elasticity,” Opt. Lett.37(10), 1625–1627 (2012).
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C. Li, Z. Huang, and R. K. Wang, “Elastic properties of soft tissue-mimicking phantoms assessed by combined use of laser ultrasonics and low coherence interferometry,” Opt. Express19(11), 10153–10163 (2011).
[CrossRef] [PubMed]

Ingram, D. R.

Izatt, J. A.

Jawad, H.

H. Jawad, A. R. Lyon, S. E. Harding, N. N. Ali, and A. R. Boccaccini, “Myocardial tissue engineering,” Br. Med. Bull.87(1), 31–47 (2008).
[CrossRef] [PubMed]

Jenkins, M. W.

John, R.

Johnson, R. L.

T. Heallen, Y. Morikawa, J. Leach, G. Tao, J. T. Willerson, R. L. Johnson, and J. F. Martin, “Hippo signaling impedes adult heart regeneration,” Development140(23), 4683–4690 (2013).
[CrossRef] [PubMed]

Johnstone, M.

Kennedy, B. F.

Kennedy, K. M.

B. F. Kennedy, K. M. Kennedy, and D. D. Sampson, “A Review of Optical Coherence Elastography: Fundamentals, Techniques and Prospects,” IEEE J. Sel. Top. Quantum Electron.20(2), 1–17 (2014).
[CrossRef]

K. M. Kennedy, C. Ford, B. F. Kennedy, M. B. Bush, and D. D. Sampson, “Analysis of mechanical contrast in optical coherence elastography,” J. Biomed. Opt.18(12), 121508 (2013).
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K. M. Kennedy, B. F. Kennedy, R. A. McLaughlin, and D. D. Sampson, “Needle optical coherence elastography for tissue boundary detection,” Opt. Lett.37(12), 2310–2312 (2012).
[CrossRef] [PubMed]

Kiehl, T.-R.

Kim, Y.

M. Xin, Y. Kim, L. B. Sutherland, M. Murakami, X. Qi, J. McAnally, E. R. Porrello, A. I. Mahmoud, W. Tan, J. M. Shelton, J. A. Richardson, H. A. Sadek, R. Bassel-Duby, and E. N. Olson, “Hippo pathway effector Yap promotes cardiac regeneration,” Proc. Natl. Acad. Sci. U.S.A.110(34), 13839–13844 (2013).
[CrossRef] [PubMed]

Kinnick, R.

S. Chen, M. W. Urban, C. Pislaru, R. Kinnick, Y. Zheng, A. Yao, and J. F. Greenleaf, “Shearwave dispersion ultrasound vibrometry (SDUV) for measuring tissue elasticity and viscosity,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control56(1), 55–62 (2009).
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Klyen, B. R.

Kochanek, K. D.

S. L. Murphy, J. Xu, and K. D. Kochanek, “Deaths: Final Data for 2010,” Natl. Vital Stat. Rep.61, 1–117 (2013).

Kolios, M. C.

Kraus, W. E.

A. B. Mathur, A. M. Collinsworth, W. M. Reichert, W. E. Kraus, and G. A. Truskey, “Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy,” J. Biomech.34(12), 1545–1553 (2001).
[CrossRef] [PubMed]

Kuznetsova, T. G.

T. G. Kuznetsova, M. N. Starodubtseva, N. I. Yegorenkov, S. A. Chizhik, and R. I. Zhdanov, “Atomic force microscopy probing of cell elasticity,” Micron38(8), 824–833 (2007).
[CrossRef] [PubMed]

Larin, K. V.

Larina, I. V.

Lazar, A. J.

Leach, J.

T. Heallen, Y. Morikawa, J. Leach, G. Tao, J. T. Willerson, R. L. Johnson, and J. F. Martin, “Hippo signaling impedes adult heart regeneration,” Development140(23), 4683–4690 (2013).
[CrossRef] [PubMed]

Lev, D. C.

Li, C.

Li, J.

S. Wang, K. V. Larin, J. Li, S. Vantipalli, R. K. Manapuram, S. Aglyamov, S. Emelianov, and M. D. Twa, “A focused air-pulse system for optical-coherence-tomography-based measurements of tissue elasticity,” Laser Phys. Lett.10(7), 075605 (2013).
[CrossRef]

S. Wang, J. Li, R. K. Manapuram, F. M. Menodiado, D. R. Ingram, M. D. Twa, A. J. Lazar, D. C. Lev, R. E. Pollock, and K. V. Larin, “Noncontact measurement of elasticity for the detection of soft-tissue tumors using phase-sensitive optical coherence tomography combined with a focused air-puff system,” Opt. Lett.37(24), 5184–5186 (2012).
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Li, P.

Liang, H. D.

P. N. Wells and H. D. Liang, “Medical ultrasound: imaging of soft tissue strain and elasticity,” J. R. Soc. Interface8(64), 1521–1549 (2011).
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Liang, X.

Lieber, M. L.

R. M. Setser, N. G. Smedira, M. L. Lieber, E. D. Sabo, and R. D. White, “Left ventricular torsional mechanics after left ventricular reconstruction surgery for ischemic cardiomyopathy,” J. Thorac. Cardiovasc. Surg.134(4), 888–896 (2007).
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Liebling, M.

I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Sequential Turning Acquisition and Reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures,” Biomed. Opt. Express3(3), 650–660 (2012).
[CrossRef] [PubMed]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt.10(5), 054001 (2005).
[CrossRef] [PubMed]

Liu, G.

W. Qi, R. Chen, L. Chou, G. Liu, J. Zhang, Q. Zhou, and Z. Chen, “Phase-resolved acoustic radiation force optical coherence elastography,” J. Biomed. Opt.17(11), 110505 (2012).
[CrossRef] [PubMed]

Luk, T. W. H.

Lyon, A. R.

H. Jawad, A. R. Lyon, S. E. Harding, N. N. Ali, and A. R. Boccaccini, “Myocardial tissue engineering,” Br. Med. Bull.87(1), 31–47 (2008).
[CrossRef] [PubMed]

Mahmoud, A. I.

M. Xin, Y. Kim, L. B. Sutherland, M. Murakami, X. Qi, J. McAnally, E. R. Porrello, A. I. Mahmoud, W. Tan, J. M. Shelton, J. A. Richardson, H. A. Sadek, R. Bassel-Duby, and E. N. Olson, “Hippo pathway effector Yap promotes cardiac regeneration,” Proc. Natl. Acad. Sci. U.S.A.110(34), 13839–13844 (2013).
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Supplementary Material (1)

» Media 1: MP4 (1929 KB)     

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Figures (6)

Fig. 1
Fig. 1

Imaging approach. (a) Schematic of SWI-OCT system setup that combines a focused air-puff device and phase-sensitive Fourier domain OCT. M-mirror; AL-achromatic lens; FC-fiber connector; FOC-fiber optics coupler; PC-polarization controller; C-collimator; SL-scan lens; TG-transmission grating; A-aperture; GM-galvanometer mirror. (b) En-face structural image from the OCT system showing the relative position and direction among the muscle fiber orientation, the air-puff port and the scanning line. The dashed lines contour the air-puff port. The SWI-OCT scanning line and the muscle fiber orientation are also called out. Scale bar corresponds to 0.5 mm.

Fig. 2
Fig. 2

Quantification of shear wave velocity. (a) The typical temporal displacement profiles from one particular depth in a tissue-mimicking phantom with 0.75% agar concentration. The magnitude of deformation at each spatial location is normalized to the absolute value of its minimum over time. (b) The plot of the data from cross-correlation of the displacement profiles in (a) in the domain of the time delay versus the shear wave propagation distance. Linear fit is applied to the data for the quantification of wave group velocity. (c) A typical example of the cross-correlation of the wave propagation signals from the mouse cardiac muscle tissue.

Fig. 3
Fig. 3

Young’s moduli quantified from SWI-OCT for the tissue-mimicking phantoms with 1%, 0.75% and 0.5% agar concentrations, compared with the results from uniaxial compression tests. Number of samples N = 3 for all measurements.

Fig. 4
Fig. 4

The 2-D depth-resolved reconstruction of shear wave propagation in the cardiac muscle tissues from (a) control and (b) CKO Lats1/2 mice (Media 1). The magnitude of deformation at each spatial location is normalized to the absolute value of its minimum over time. Scale bars correspond to 0.5 mm. The red dots represent the air-puff excitation positions on both tissue samples.

Fig. 5
Fig. 5

Plots of the shear wave propagation distance versus the time delay at typical depths for the myocardium from (a) control and (b) CKO Lats1/2 mice. The magnitude of deformation at each spatial location is normalized to the absolute value of its minimum over time. The time axes indicate the shear wave propagation with the time delay forming over spatial locations.

Fig. 6
Fig. 6

The SWI-OCT measurements reveal lower stiffness in Lats1/2 deficient cardiac tissues. (a) Shear wave velocities and (b) Young’s moduli of cardiac muscle tissues from control and CKO Lats1/2 mice. * p<0.05 from unpaired two-sample student’s t-test. Number of samples N = 3 for control and N = 4 for CKO Lats1/2 mice.

Equations (3)

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μ=ρ C 2 ,
E=2(1+ν)μ,
E=3ρ C 2 .

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