Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2016 (2016), Article ID 6893712, 11 pages
http://dx.doi.org/10.1155/2016/6893712
Research Article

Cross-Sectional Nakagami Images in Passive Stretches Reveal Damage of Injured Muscles

1Department of Biomedical Engineering, National Cheng Kung University, No. 1, University Road, Tainan 701, Taiwan
2Department of Computer Science and Information Engineering, National Cheng Kung University, No. 1, University Road, Tainan 701, Taiwan
3Department of Occupational Therapy, I-Shou University, No. 1, Sec. 1, Syuecheng Road, Dashu District, Kaohsiung, Taiwan
4Department of Cell Biology and Anatomy, National Cheng Kung University, No. 1, University Road, Tainan 701, Taiwan
5Institute of Basic Medical Sciences, National Cheng Kung University, No. 1, University Road, Tainan 701, Taiwan
6Department of Biomedical Engineering, University of Southern California, Los Angeles, CA 90089, USA
7Medical Device and Innovation Center, National Cheng Kung University, No. 1, University Road, Tainan 701, Taiwan

Received 13 August 2015; Revised 5 November 2015; Accepted 9 November 2015

Academic Editor: Bo Zuo

Copyright © 2016 Shih-Ping Lin et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Orchard, “Biomechanics of muscle strain injury,” New Zealand Journal of Sports Medicine, vol. 30, pp. 90–97, 2002. View at Google Scholar
  2. A. J. Ryan, “Quadriceps strain, rupture and charlie horse,” Medicine & Science in Sports & Exercise, vol. 1, pp. 106–111, 1969. View at Google Scholar
  3. D. C. Taylor, J. D. Dalton Jr., A. V. Seaber, and W. E. Garrett Jr., “Viscoelastic properties of muscle-tendon units,” The American Journal of Sports Medicine, vol. 18, no. 3, pp. 300–309, 1990. View at Publisher · View at Google Scholar · View at Scopus
  4. Y. C. Fung, Biomechanics: Mechanical Properties of Living Tissues, Springer, New York, NY, USA, 2nd edition, 1993.
  5. G. A. Meyer, A. D. McCulloch, and R. L. Lieber, “A nonlinear model of passive muscle viscosity,” Journal of Biomechanical Engineering, vol. 133, no. 9, Article ID 091007, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. A. R. Gillies and R. L. Lieber, “Structure and function of the skeletal muscle extracellular matrix,” Muscle & Nerve, vol. 44, no. 3, pp. 318–331, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Hete and K. K. Shung, “Scattering of ultrasound from skeletal muscle tissue,” IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, vol. 40, no. 4, pp. 354–365, 1993. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Light and A. E. Champion, “Characterization of muscle epimysium, perimysium and endomysium collagens,” The Biochemical Journal, vol. 219, no. 3, pp. 1017–1026, 1984. View at Publisher · View at Google Scholar · View at Scopus
  9. P. K. Nikolaou, B. L. Macdonald, R. R. Glisson, A. V. Seaber, and W. E. Garrett Jr., “Biomechanical and histological evaluation of muscle after controlled strain injury,” American Journal of Sports Medicine, vol. 15, no. 1, pp. 9–14, 1987. View at Publisher · View at Google Scholar · View at Scopus
  10. D. R. Armfield, D. H. Kim, J. D. Towers, J. P. Bradley, and D. D. Robertson, “Sports-related muscle injury in the lower extremity,” Clinics in Sports Medicine, vol. 25, no. 4, pp. 803–842, 2006. View at Publisher · View at Google Scholar
  11. O. Chan, A. Del Buono, T. M. Best, and N. Maffulli, “Acute muscle strain injuries: a proposed new classification system,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 20, no. 11, pp. 2356–2362, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. T. J. Noonan and W. E. Garrett Jr., “Muscle strain injury: diagnosis and treatment,” The Journal of the American Academy of Orthopaedic Surgeons, vol. 7, no. 4, pp. 262–269, 1999. View at Google Scholar · View at Scopus
  13. N. Ahmad, M. Bygrave, R. Chhem et al., “High-frequency ultrasound to grade disease progression in murine models of Duchenne muscular dystrophy,” Journal of Ultrasound in Medicine, vol. 28, no. 6, pp. 707–716, 2009. View at Google Scholar · View at Scopus
  14. H. H. Kim, J. M. Cannata, R. Liu, J. H. Chang, R. H. Silverman, and K. K. Shung, “20 MHz/40 MHz dual element transducers for high frequency harmonic imaging,” IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, vol. 55, no. 12, pp. 2683–2691, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. J. M. Cannata, T. A. Ritter, W.-H. Chen, R. H. Silverman, and K. K. Shung, “Design of efficient, broadband single-element (20–80 MHz) ultrasonic transducers for medical imaging applications,” IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, vol. 50, no. 11, pp. 1548–1557, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. Q. Q. Zhang, F. T. Djuth, Q. F. Zhou, C. H. Hu, J. H. Cha, and K. K. Shung, “High frequency broadband PZT thick film ultrasonic transducers for medical imaging applications,” Ultrasonics, vol. 44, supplement, pp. e711–e715, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. Y.-C. Chen, Y.-H. Lin, S.-H. Wang, S.-P. Lin, K. K. Shung, and C.-C. Wu, “Monitoring tissue inflammation and responses to drug treatments in early stages of mice bone fracture using 50 MHz ultrasound,” Ultrasonics, vol. 54, no. 1, pp. 177–186, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. M.-C. Ho, J.-J. Lin, Y.-C. Shu et al., “Using ultrasound Nakagami imaging to assess liver fibrosis in rats,” Ultrasonics, vol. 52, no. 2, pp. 215–222, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. H. Lin, C. C. Huang, and S. H. Wang, “Quantitative assessments of burn degree by high-frequency ultrasonic backscattering and statistical model,” Physics in Medicine and Biology, vol. 56, no. 3, pp. 757–773, 2011. View at Publisher · View at Google Scholar
  20. Y.-H. Lin, C.-C. Huang, and S.-H. Wang, “Quantitative assessment on the orientation and distribution of carbon fibers in a conductive polymer composite using high-frequency ultrasound,” IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, vol. 59, no. 5, pp. 970–980, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. Y.-Y. Liao, C.-H. Li, P.-H. Tsui et al., “Strain-compounding technique with ultrasound Nakagami imaging for distinguishing between benign and malignant breast tumors,” Medical Physics, vol. 39, no. 5, pp. 2325–2333, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. Z. Zhou, S. Wu, C.-Y. Wang, H.-Y. Ma, C.-C. Lin, and P.-H. Tsui, “Monitoring radiofrequency ablation using real-time ultrasound nakagami imaging combined with frequency and temporal compounding techniques,” PLoS ONE, vol. 10, no. 2, Article ID e0118030, 2015. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Rana and J. M. Wakeling, “In-vivo determination of 3D muscle architecture of human muscle using free hand ultrasound,” Journal of Biomechanics, vol. 44, no. 11, pp. 2129–2135, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. R. B. Armstrong, G. L. Warren, and J. A. Warren, “Mechanisms of exercise-induced muscle fibre injury,” Sports Medicine, vol. 12, no. 3, pp. 184–207, 1991. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Duenwald, H. Kobayashi, K. Frisch, R. Lakes, and R. Vanderby, “Ultrasound echo is related to stress and strain in tendon,” Journal of Biomechanics, vol. 44, no. 3, pp. 424–429, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Duenwald-Kuehl, R. Lakes, and R. Vanderby Jr., “Strain-induced damage reduces echo intensity changes in tendon during loading,” Journal of Biomechanics, vol. 45, no. 9, pp. 1607–1611, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Duenwald-Kuehl, J. Kondratko, R. S. Lakes, and R. Vanderby, “Damage mechanics of porcine flexor tendon: mechanical evaluation and modeling,” Annals of Biomedical Engineering, vol. 40, no. 8, pp. 1692–1707, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. L. G. Prado, I. Makarenko, C. Andresen, M. Krüger, C. A. Opitz, and W. A. Linke, “Isoform diversity of giant proteins in relation to passive and active contractile properties of rabbit skeletal muscles,” The Journal of General Physiology, vol. 126, no. 5, pp. 461–480, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. S. R. Ward, A. Tomiya, G. J. Regev et al., “Passive mechanical properties of the lumbar multifidus muscle support its role as a stabilizer,” Journal of Biomechanics, vol. 42, no. 10, pp. 1384–1389, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. P. P. Purslow, “The structure and functional significance of variations in the connective tissue within muscle,” Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, vol. 133, no. 4, pp. 947–966, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. A. R. Gillies, L. R. Smith, R. L. Lieber, and S. Varghese, “Method for decellularizing skeletal muscle without detergents or proteolytic enzymes,” Tissue Engineering Part C: Methods, vol. 17, no. 4, pp. 383–389, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. G. A. Meyer and R. L. Lieber, “Elucidation of extracellular matrix mechanics from muscle fibers and fiber bundles,” Journal of Biomechanics, vol. 44, no. 4, pp. 771–773, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. V. Twersky, “Low-frequency scattering by correlated distributions of randomly oriented particles,” The Journal of the Acoustical Society of America, vol. 81, no. 5, pp. 1609–1678, 1987. View at Publisher · View at Google Scholar
  34. C.-Y. Wang and K. K. Shung, “Variation in ultrasonic backscattering from skeletal muscle during passive stretching,” IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, vol. 45, no. 2, pp. 504–510, 1998. View at Publisher · View at Google Scholar · View at Scopus
  35. R. J. Baskin and P. Paolini, “Volume change accompanying passive stretch of frog muscle,” Nature, vol. 204, no. 4959, pp. 694–695, 1964. View at Publisher · View at Google Scholar · View at Scopus
  36. R. K. Saha and M. C. Kolios, “Effects of cell spatial organization and size distribution on ultrasound backscattering,” IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, vol. 58, no. 10, pp. 2118–2131, 2011. View at Publisher · View at Google Scholar · View at Scopus