Three-dimensional optical coherence microelastography of skeletal muscle tissue

Biomedical Optics Express

Volumn 5, Issue 9, 2014, Pages 3090-3102

  Chin, Lixin ^a   Kennedy, Brendan F ^a   Kennedy, Kelsey M ^a   Wijesinghe, Philip ^a   Pinniger, Gavin J ^a   Terrill, Jessica R ^a   McLaughlin, Robert A ^a   Sampson, David D ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; MECHANICAL PROPERTIES; MEDICAL IMAGING; MUSCLE; MUSCULOSKELETAL SYSTEM; OPTICAL TOMOGRAPHY; PATHOLOGY;

DUCHENNE MUSCULAR DYSTROPHIES; ELASTOGRAPHY; MECHANICAL LOADS; MOUSE MODELS; MUSCLE TISSUES; QUASI-STATIC; SKELETAL MUSCLE;

TISSUE;

ANIMAL MODEL; DISEASE MODEL; ELASTOGRAPHY; MODEL; MUSCLE TISSUE; OPTICAL COHERENCE TOMOGRAPHY; SKELETAL MUSCLE; TENDON; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

EID: 84913605908     PISSN: None     EISSN: 21567085     Source Type: Journal    
DOI: 10.1364/BOE.5.003090     Document Type: Article

References (54)

1. V. M. Zatsiorsky and B. I. Prilutsky, Biomechanics of Skeletal Muscles (Human Kinetics, 2012).
2. H. Maas and T. G. Sandercock, “Force transmission between synergistic skeletal muscles through connective tissue linkages,” J. Biomed. Biotechnol. 2010, 575672 (2010).
3. G. J. Pinniger, K. W. Ranatunga, and G. W. Offer, “Crossbridge and non-crossbridge contributions to tension in lengthening rat muscle: force-induced reversal of the power stroke,” J. Physiol. 573(3), 627–643 (2006).
4. J. R. H. Foran, S. Steinman, I. Barash, H. G. Chambers, and R. L. Lieber, “Structural and mechanical alterations in spastic skeletal muscle,” Dev. Med. Child Neurol. 47(10), 713–717 (2005).
5. C. H. Hakim, R. W. Grange, and D. Duan, “The passive mechanical properties of the extensor digitorum longus muscle are compromised in 2- to 20-mo-old mdx mice,” J. Appl. Physiol. 110(6), 1656–1663 (2011).
6. K. Bushby, R. Finkel, D. J. Birnkrant, L. E. Case, P. R. Clemens, L. Cripe, A. Kaul, K. Kinnett, C. McDonald, S. Pandya, J. Poysky, F. Shapiro, J. Tomezsko, and C. Constantin; DMD Care Considerations Working Group, “Diagnosis and management of Duchenne muscular dystrophy, Part 1: Diagnosis, and pharmacological and psychosocial management,” Lancet Neurol. 9(1), 77–93 (2010).
7. E. E. Zubrzycka-Gaarn, D. E. Bulman, G. Karpati, A. H. M. Burghes, B. Belfall, H. J. Klamut, J. Talbot, R. S. Hodges, P. N. Ray, and R. G. Worton, “The Duchenne muscular dystrophy gene product is localized in sarcolemma of human skeletal muscle,” Nature 333(6172), 466–469 (1988).
8. M. J. Spencer and J. G. Tidball, “Do immune cells promote the pathology of dystrophin-deficient myopathies?” Neuromuscul. Disord. 11(6-7), 556–564 (2001).
9. T. Shavlakadze, J. White, J. F. Y. Hoh, N. Rosenthal, and M. D. Grounds, “Targeted expression of insulin-like growth factor-I reduces early myofiber necrosis in dystrophic mdx mice,” Mol. Ther. 10(5), 829–843 (2004).
10. M. Canato, M. Dal Maschio, F. Sbrana, R. Raiteri, C. Reggiani, S. Vassanelli, and A. Megighian, “Mechanical and electrophysiological properties of the sarcolemma of muscle fibers in two murine models of muscle dystrophy: Col6a1-/- and mdx,” J. Biomed. Biotechnol. 2010, 981945 (2010).
11. K. P. García-Pelagio, R. J. Bloch, A. Ortega, and H. González-Serratos, “Biomechanics of the sarcolemma and costameres in single skeletal muscle fibers from normal and dystrophin-null mice,” J. Muscle Res. Cell Motil. 31(5-6), 323–336 (2011).
12. E. E. Drakonaki and G. M. Allen, “Magnetic resonance imaging, ultrasound and real-time ultrasound elastography of the thigh muscles in congenital muscle dystrophy,” Skeletal Radiol. 39(4), 391–396 (2010).
13. K. J. Parker, M. M. Doyley, and D. J. Rubens, “Imaging the elastic properties of tissue: the 20 year perspective,” Phys. Med. Biol. 56(1), R1–R29 (2011).
14. F. Cornelio and I. Dones, “Muscle fiber degeneration and necrosis in muscular dystrophy and other muscle diseases: cytochemical and immunocytochemical data,” Ann. Neurol. 16(6), 694–701 (1984).
15. G. R. Coulton, J. E. Morgan, T. A. Partridge, and J. C. Sloper, “The mdx mouse skeletal muscle myopathy: I. A histological, morphometric and biochemical investigation,” Neuropathol. Appl. Neurobiol. 14(1), 53–70 (1988).
16. J. M. Schmitt, “OCT elastography: imaging microscopic deformation and strain of tissue,” Opt. Express 3(6), 199–211 (1998).
17. 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), 7101217 (2014).
18. B. F. Kennedy, K. M. Kennedy, A. L. Oldenburg, S. G. Adie, S. A. Boppart, and D. D. Sampson, “Optical coherence elastography,” in Optical Coherence Tomography: Technology and Applications, J. G. Fujimoto, and W. Drexler, eds. (Springer, to be published).
19. 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).
20. 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).
21. A. Nahas, M. Bauer, S. Roux, and A. C. Boccara, “3D static elastography at the micrometer scale using full field OCT,” Biomed. Opt. Express 4(10), 2138–2149 (2013).
22. V. Crecea, A. Ahmad, and S. A. Boppart, “Magnetomotive optical coherence elastography for microrheology of biological tissues,” J. Biomed. Opt. 18(12), 121504 (2013).
23. K. M. Kennedy, R. A. McLaughlin, B. F. Kennedy, A. Tien, B. Latham, C. M. Saunders, and D. D. Sampson, “Needle optical coherence elastography for the measurement of microscale mechanical contrast deep within human breast tissues,” J. Biomed. Opt. 18(12), 121510 (2013).
24. V. Y. Zaitsev, L. A. Matveev, A. L. Matveyev, G. V. Gelikonov, and V. M. Gelikonov, “Elastographic mapping in optical coherence tomography using an unconventional approach based on correlation stability,” J. Biomed. Opt. 19(2), 021107 (2014).
25. B. F. Kennedy, R. A. McLaughlin, K. M. Kennedy, L. Chin, A. Curatolo, A. Tien, B. Latham, C. M. Saunders, and D. D. Sampson, “Optical coherence micro-elastography: mechanical-contrast imaging of tissue microstructure,” Biomed. Opt. Express 5(7), 2113–2124 (2014).
26. 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).
27. K. E. O’Hara, T. Schmoll, C. Vass, and R. A. Leitgeb, “Measuring pulse-induced natural relative motions within human ocular tissue in vivo using phase-sensitive optical coherence tomography,” J. Biomed. Opt. 18(12), 121506 (2013).
28. N. Dragostinoff, R. M. Werkmeister, J. Klaizer, M. Gröschl, and L. Schmetterer, “Time course and topographic distribution of ocular fundus pulsation measured by low-coherence tissue interferometry,” J. Biomed. Opt. 18(12), 121502 (2013).
29. G. van Soest, F. Mastik, N. de Jong, and A. F. W. van der Steen, “Robust intravascular optical coherence elastography by line correlations,” Phys. Med. Biol. 52(9), 2445–2458 (2007).
30. 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. Express 19(7), 6623–6634 (2011).
31. L. V. Coutts, N. R. Miller, C. C. Harland, and J. C. Bamber, “Feasibility of skin surface elastography by tracking skin surface topography,” J. Biomed. Opt. 18(12), 121513 (2013).
32. C. Y. L. Chao, Y.-P. Zheng, and G. L. Y. Cheing, “A novel noncontact method to assess the biomechanical properties of wound tissue,” Wound Repair Regen. 19(3), 324–329 (2011).
33. G. Guan, C. Li, Y. Ling, Y. Yang, J. B. Vorstius, R. P. Keatch, R. K. Wang, and Z. Huang, “Quantitative evaluation of degenerated tendon model using combined optical coherence elastography and acoustic radiation force method,” J. Biomed. Opt. 18(11), 111417 (2013).
34. S. Wang, A. L. Lopez III, Y. Morikawa, G. Tao, J. Li, I. V. Larina, J. F. Martin, and K. V. Larin, “Noncontact quantitative biomechanical characterization of cardiac muscle using shear wave imaging optical coherence tomography,” Biomed. Opt. Express 5(7), 1980–1992 (2014).
35. M. D. Grounds, H. G. Radley, G. S. Lynch, K. Nagaraju, and A. De Luca, “Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy,” Neurobiol. Dis. 31(1), 1–19 (2008).
36. J. J. Pasquesi, S. C. Schlachter, M. D. Boppart, E. Chaney, S. J. Kaufman, and S. A. Boppart, “In vivo detection of exercised-induced ultrastructural changes in genetically-altered murine skeletal muscle using polarizationsensitive optical coherence tomography,” Opt. Express 14(4), 1547–1556 (2006).
37. B. R. Klyen, T. Shavlakadze, H. G. Radley-Crabb, M. D. Grounds, and D. D. Sampson, “Identification of muscle necrosis in the mdx mouse model of Duchenne muscular dystrophy using three-dimensional optical coherence tomography,” J. Biomed. Opt. 16(7), 076013 (2011).
38. X. Yang, L. Chin, B. R. Klyen, T. Shavlakadze, R. A. McLaughlin, M. D. Grounds, and D. D. Sampson, “Quantitative assessment of muscle damage in the mdx mouse model of Duchenne muscular dystrophy using polarization-sensitive optical coherence tomography,” J. Appl. Physiol. 115(9), 1393–1401 (2013).
39. X. Yang, D. Lorenser, R. A. McLaughlin, R. W. Kirk, M. Edmond, M. C. Simpson, M. D. Grounds, and D. D. Sampson, “Imaging deep skeletal muscle structure using a high-sensitivity ultrathin side-viewing optical coherence tomography needle probe,” Biomed. Opt. Express 5(1), 136–148 (2014).
40. 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. Express 5(4), 1217–1232 (2014).
41. 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).
42. 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. Express 17(24), 21762–21772 (2009).
43. 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).
44. B. F. Kennedy, S. H. Koh, R. A. McLaughlin, K. M. Kennedy, P. R. T. Munro, and D. D. Sampson, “Strain estimation in phase-sensitive optical coherence elastography,” Biomed. Opt. Express 3(8), 1865–1879 (2012).
45. H. G. Radley-Crabb, J. Terrill, T. Shavlakadze, J. Tonkin, P. Arthur, and M. D. Grounds, “A single 30 min treadmill exercise session is suitable for ‘proof-of concept studies’ in adult mdx mice: a comparison of the early consequences of two different treadmill protocols,” Neuromuscul. Disord. 22(2), 170–182 (2012).
46. L. F. B. Torres and L. W. Duchen, “The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates,” Brain 110(2), 269–299 (1987).
47. T. Varghese and J. Ophir, “A theoretical framework for performance characterization of elastography: the strain filter,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control 44(1), 164–172 (1997).
48. A. R. Gillies and R. L. Lieber, “Structure and function of the skeletal muscle extracellular matrix,” Muscle Nerve 44(3), 318–331 (2011).
49. M. P. E. Wenger, L. Bozec, M. A. Horton, and P. Mesquida, “Mechanical properties of collagen fibrils,” Biophys. J. 93(4), 1255–1263 (2007).
50. K. A. Ramsey, A. J. Bakker, and G. J. Pinniger, “Fiber-type dependence of stretch-induced force enhancement in rat skeletal muscle,” Muscle Nerve 42(5), 769–777 (2010).
51. K. S. Ramaswamy, M. L. Palmer, J. H. van der Meulen, A. Renoux, T. Y. Kostrominova, D. E. Michele, and J. A. Faulkner, “Lateral transmission of force is impaired in skeletal muscles of dystrophic mice and very old rats,” J. Physiol. 589(5), 1195–1208 (2011).
52. B. F. Kennedy, F. G. Malheiro, L. Chin, and D. D. Sampson, “Three-dimensional optical coherence elastography by phase-sensitive comparison of C-scans,” J. Biomed. Opt. 19(7), 076006 (2014).
53. K. M. Kennedy, S. Es’haghian, L. Chin, R. A. McLaughlin, D. D. Sampson, and B. F. Kennedy, “Optical palpation: optical coherence tomography-based tactile imaging using a compliant sensor,” Opt. Lett. 39(10), 3014–3017 (2014).
54. 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).