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Therapeutic Effects of Multimodal Biophysical Stimulation on Muscle Atrophy in a Mouse Model

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Abstract

Muscle atrophy is defined as the decrease in the size and number of muscle fibers, and is associated with injury to muscle structures. Recently, biophysical therapies using laser, ultrasound, and vibration has been widely used to improve muscle atrophy. However, although the effects of these stimuli seem to be similar, the mechanisms by which they stimulate biological tissue may be different. From this point of view, we expected that it would be possible to produce synergetic effects through combining these three different types of biophysical stimuli on biological tissues, based on the therapeutic benefit of each stimulus. For this, 35 males, 12-week old, C57BL/6 mice (21 ± 1.2 g), were randomly assigned to five groups: a) a sciatic nerve neurectomized “control” group (C, n = 7), b) a MILNS (Minimally Invasive Laser Needle System) therapy after sciatic nerve neurectomized group (L, n = 7), c) a LIPUS (Low-Intensity Pulsed Ultrasound) therapy after sciatic nerve neurectomized group (U, n = 7), e) a PVS (Partial Vibration Stimulation) therapy after sciatic nerve neurectomized group (V, n = 7), and e) a multimodal biophysical stimulation after sciatic nerve neurectomized group (MS, n = 7).

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References

  1. Hong, S. and Choi, W. H., “Clinical and Physiopathological Mechanism of Sarcopenia,” The Korean Journal of Medicine, Vol. 83, No. 4, pp. 444–454, 2012.

    Article  Google Scholar 

  2. Järvinen, T. A., Järvinen, T. L., Kääriäinen, M., Kalimo, H., and Järvinen, M., “Muscle Injuries: Biology and Treatment,” The American Journal of Sports Medicine, Vol. 33, No. 5, pp. 745–764, 2005.

    Article  Google Scholar 

  3. Mônico-Neto, M., Antunes, H. K. M., Dattilo, M., Medeiros, A., Souza, H. S. D., et al., “Resistance Exercise: A Non-Pharmacological Strategy to Minimize or Reverse Sleep Deprivation-Induced Muscle Atrophy,” Medical Hypotheses, Vol. 80, No. 6, pp. 701–705, 2013.

    Article  Google Scholar 

  4. Kouidi, E., Albani, M., Natsis, K., Megalopoulos, A., Gigis, P., Guiba-Tziampiri, O., et al., “The Effects of Exercise Training on Muscle Atrophy in Haemodialysis Patients,” Nephrology, Dialysis, Transplantation: Official Publication of the European Dialysis and Transplant Association-European Renal Association, Vol. 13, No. 3, pp. 685–699, 1998.

    Article  Google Scholar 

  5. Huard, J., Cao, B., and Qu-Petersen, Z., “Muscle-Derived Stem Cells: Potential for Muscle Regeneration,” Birth Defects Research Part C: Embryo Today: Reviews, Vol. 69, No. 3, pp. 230–237, 2003.

    Article  Google Scholar 

  6. Qu-Petersen, Z., Deasy, B., Jankowski, R., Ikezawa, M., Cummins, J., Pruchnic, R., Mytinger, J., Cao, B., Gates, C., and Wernig, A., “Identification of a Novel Population of Muscle Stem Cells in Mice: Potential for Muscle Regeneration,” The Journal of Cell Biology, Vol. 157, No. 5, pp. 851–864, 2002.

    Article  Google Scholar 

  7. Brown, E. S., Khan, D. A., and Nejtek, V. A., “The Psychiatric Side Effects of Corticosteroids,” Annals of Allergy, Asthma & Immunology, Vol. 83, No. 6, pp. 495–504, 1999.

    Article  Google Scholar 

  8. Gerber, J. P., Marcus, R. L., Dibble, L. E., Greis, P. E., Burks, R. T., and LaStayo, P. C., “Effects of Early Progressive Eccentric Exercise on Muscle Structure after Anterior Cruciate Ligament Reconstruction,” Journal of Bone and Joint Surgery, Vol. 89, No. 3, pp. 559–570, 2007.

    Article  Google Scholar 

  9. van der Windt, D. A., van der Heijden, G. J., van den Berg, S. G., ter Riet, G., de Winter, A. F., and Bouter, L. M., “Ultrasound Therapy for Musculoskeletal Disorders: A Systematic Review,” Pain, Vol. 81, No. 3, pp. 257–271, 1999.

    Article  Google Scholar 

  10. Alves, A. N., Fernandes, K. P. S., Deana, A. M., Bussadori, S. K., and Mesquita-Ferrari, R. A., “Effects of Low-Level Laser Therapy on Skeletal Muscle Repair: A Systematic Review,” American Journal of Physical Medicine & Rehabilitation, Vol. 93, No. 12, pp. 1073–1085, 2014.

    Article  Google Scholar 

  11. Blottner, D., Salanova, M., Püttmann, B., Schiffl, G., Felsenberg, D., et al., “Human Skeletal Muscle Structure and Function Preserved by Vibration Muscle Exercise Following 55 Days of Bed Rest,” European Journal of Applied Physiology, Vol. 97, No. 3, pp. 261–271, 2006.

    Article  Google Scholar 

  12. Assis, L., Moretti, A. I. S., Abrahão, T. B., de Souza, H. P., Hamblin, M. R., and Parizotto, N. A., “Low-Level Laser Therapy (808 Nm) Contributes to Muscle Regeneration and Prevents Fibrosis in Rat Tibialis Anterior Muscle after Cryolesion,” Lasers in Medical Science, Vol. 28, No. 3, pp. 947–955, 2013.

    Article  Google Scholar 

  13. Nakano, J., Kataoka, H., Sakamoto, J., Origuchi, T., Okita, M., and Yoshimura, T., “Low-Level Laser Irradiation Promotes the Recovery of Atrophied Gastrocnemius Skeletal Muscle in Rats,” Experimental physiology, Vol. 94, No. 9, pp. 1005–1015, 2009.

    Article  Google Scholar 

  14. Pertille, A., Macedo, A. B., and Oliveira, C. P., “Evaluation of Muscle Regeneration in Aged Animals after Treatment with Low-Level Laser Therapy,” Brazilian Journal of Physical Therapy, Vol. 16, No. 6, pp. 495–501, 2012.

    Article  Google Scholar 

  15. Ninomiya, T., Hosoya, A., Nakamura, H., Sano, K., Nishisaka, T., and Ozawa, H., “Increase of Bone Volume by a Nanosecond Pulsed Laser Irradiation is Caused by a Decreased Osteoclast Number and an Activated Osteoblasts,” Bone, Vol. 40, No. 1, pp. 140–148, 2007.

    Article  Google Scholar 

  16. Huang, Y. Y., Chen, A. C.-H., Carroll, J. D., and Hamblin, M. R., “Biphasic Dose Response in Low Level Light Therapy,” Dose Response, Vol. 7, No. 4, pp. 358–383, 2009.

    Article  Google Scholar 

  17. Rantanen, J., Thorsson, O., Wollmer, P., Hurme, T., and Kalimo, H., “Effects of Therapeutic Ultrasound on the Regeneration of Skeletal Myofibers after Experimental Muscle Injury,” The American Journal of Sports Medicine, Vol. 27, No. 1, pp. 54–59, 1999.

    Article  Google Scholar 

  18. Ziskin, M. C., “Applications of Ultrasound in Medicine - Comparison with Other Modalities,” in: Ultrasound, Repacholi M. H., Grandolfo M., Rindi A., (Eds.), Springer, pp. 49-59, 1987.

  19. Brown, B., “How Safe is Diagnostic Ultrasonography?” Canadian Medical Association Journal, Vol. 131, No. 4, pp. 307–311, 1984.

    Google Scholar 

  20. Drastichova, V., Samohyl, J., and Slavetinska, A., “Strengthening of Sutured Skin Wound with Ultrasound in Experiments of Animals,” Plastic and Reconstructive Surgery, Vol. 53, No. 5, pp. 611, 1974.

    Article  Google Scholar 

  21. Miller, D. L., Smith, N. B., Bailey, M. R., Czarnota, G. J., Hynynen, K., et al., “Overview of Therapeutic Ultrasound Applications and Safety Considerations,” Journal of Ultrasound in Medicine, Vol. 31, No. 4, pp. 623–634, 2012.

    Article  Google Scholar 

  22. Enwemeka, C. S., Rodriguez, O., and Mendosa, S., “The Biomechanical Effects of Low-Intensity Ultrasound on Healing Tendons,” Ultrasound in Medicine & Biology, Vol. 16, No. 8, pp. 801–807, 1990.

    Article  Google Scholar 

  23. Frieder, S., Weisberg, J., Fleming, B., and Stanek, A., “A Pilot Study: The Therapeutic Effect of Ultrasound Following Partial Rupture of Achilles Tendons in Male Rats,” Journal of Orthopaedic & Sports Physical Therapy, Vol. 10, No. 2, pp. 39–46, 1988.

    Article  Google Scholar 

  24. Qin, L., Lu, H., Fok, P., Cheung, W., Zheng, Y., Lee, K., and Leung, K., “Low-Intensity Pulsed Ultrasound Accelerates Osteogenesis at Bone-Tendon Healing Junction,” Ultrasound in Medicine & Biology, Vol. 32, No. 12, pp. 1905–1911, 2006.

    Article  Google Scholar 

  25. Walsh, W. R., Stephens, P., Vizesi, F., Bruce, W., Huckle, J., and Yu, Y., “Effects of Low-Intensity Pulsed Ultrasound on Tendon-Bone Healing in an Intra-Articular Sheep Knee Model,” Arthroscopy: The Journal of Arthroscopic & Related Surgery, Vol. 23, No. 2, pp. 197–204, 2007.

    Article  Google Scholar 

  26. Klug, W., Franke, W.-G., and Knoch, H.-G., “Scintigraphic Control of Bone-Fracture Healing under Ultrasonic Stimulation: An Animal Experimental Study,” European Journal of Nuclear Medicine, Vol. 11, No. 12, pp. 494–497, 1986.

    Article  Google Scholar 

  27. Pilla, A., Mont, M., Nasser, P., Khan, S., Figueiredo, M., Kaufman, J., and Siffert, R., “Non-Invasive Low-Intensity Pulsed Ultrasound Accelerates Bone Healing in the Rabbit,” Journal of Orthopaedic Trauma, Vol. 4, No. 3, pp. 246–253, 1990.

    Article  Google Scholar 

  28. Cronin, J. B., Oliver, M., and McNair, P. J., “Muscle Stiffness and Injury Effects of Whole Body Vibration,” Physical Therapy in Sport, Vol. 5, No. 2, pp. 68–74, 2004.

    Article  Google Scholar 

  29. Kosar, A. C., Candow, D. G., and Putland, J. T., “Potential Beneficial Effects of Whole-Body Vibration for Muscle Recovery After Exercise,” The Journal of Strength & Conditioning Research, Vol. 26, No. 10, pp. 2907–2911, 2012.

    Article  Google Scholar 

  30. Cardinale, M. and Pope, M. H., “The Effects of Whole Body Vibration on Humans: Dangerous or Advantageous?” Acta Physiologica Hungarica, Vol. 90, No. 3, pp. 195–206, 2003.

    Article  Google Scholar 

  31. Paddan, G. S. and Griffin, M. J., “A Review of the Transmission of Translational Seat Vibration to the Head,” Journal of Sound and Vibration, Vol. 215, No. 4, pp. 863–882, 1998.

    Article  Google Scholar 

  32. Pope, M. H., Wilder, D. G., and Magnusson, M., “Possible Mechanisms of Low Back Pain due to Whole-Body Vibration,” Journal of Sound and Vibration, Vol. 215, No. 4, pp. 687–697, 1998.

    Article  Google Scholar 

  33. Park, J. H., Seo, D.-H., Cho, S., Kim, S.-H., Eom, S., and Kim, H. S., “Effects of Partial Vibration on Morphological Changes in Bone and Surrounding Muscle of Rats under Microgravity Condition: Comparative Study by Gender,” Microgravity Science and Technology, Vol. 27, No. 5, pp. 361–368, 2015.

    Article  Google Scholar 

  34. Karshafian, R., Bevan, P. D., Williams, R., Samac, S., and Burns, P. N., “Sonoporation by Ultrasound-Activated Microbubble Contrast Agents: Effect of acoustic Exposure Parameters on Cell Membrane Permeability and Cell Viability,” Ultrasound in Medicine & Biology, Vol. 35, No. 5, pp. 847–860, 2009.

    Article  Google Scholar 

  35. Lee, Y.-H., Kim, W.-J., Lee, M.-H., Kim, S.-Y., Seo, D.-H., et al., “Anti-Skeletal Muscle Atrophy Effect of Oenothera Odorata Root Extract via Reactive Oxygen Species-Dependent Signaling Pathways in Cellular and Mouse Model,” Bioscience, Biotechnology, and Biochemistry, Vol. 80, No. 1, pp. 80–88, 2016.

    Article  Google Scholar 

  36. Rhee, M.-H. and Kim, J.-S., “Muscle Recovery after Sciatic Nerve Crush Injury in Rats by Different Loading Swimming Exercise,” Journal of the Korean Society of Physical Medicine, Vol. 8, No. 4, pp. 525–532, 2013.

    Article  Google Scholar 

  37. Choe, M., Kim, K.-H., An, G.-J., Lee, K.-S., and Choi, J.-A., “Hindlimb Muscle Atrophy of Rat Induced by Neuropathic Pain,” Journal of Korean Biological Nursing Science, Vol. 10, No. 1, pp. 88–95, 2008.

    Google Scholar 

  38. Nader, G. A., “Molecular Determinants of Skeletal Muscle Mass: Getting the “AKT” Together,” The International Journal of Biochemistry & Cell Biology, Vol. 37, No. 10, pp. 1985–1996, 2005.

    Article  Google Scholar 

  39. Furuno, K., Goodman, M. N., and Goldberg, A. L., “Role of Different Proteolytic Systems in the Degradation of Muscle Proteins during Denervation Atrophy,” Journal of Biological Chemistry, Vol. 265, No. 15, pp. 8550–8557, 1990.

    Google Scholar 

  40. Goldberg, A. L., “Protein Turnover in Skeletal Muscle II. Effects of Denervation and Cortisone on Protein Catabolism in Skeletal Muscle,” Journal of Biological Chemistry, Vol. 244, No. 12, pp. 3223–3229, 1969.

    Google Scholar 

  41. Yoon, B.-C., Yu, B.-K., and Lee, M.-H., “Exercise Effects on the Atrophy of Denervated Muscles in Rat,” Physical Therapy Korea, Vol. 7, No. 3, pp. 34–48, 2000.

    Google Scholar 

  42. Kim, J. I. and Choe, M., “Effects of Unilateral Sciatic Nerve Injury on Unaffected Hindlimb Muscles of Rats,” Journal of Korean Academy of Nursing, Vol. 39, No. 3, pp. 393–400, 2009.

    Article  Google Scholar 

  43. Holloszy, J. O. and Coyle, E. F., “Adaptations of Skeletal Muscle to Endurance Exercise and their Metabolic Consequences,” Journal of Applied Physiology, Vol. 56, No. 4, pp. 831–838, 1984.

    Article  Google Scholar 

  44. Wisdom, K. M., Delp, S. L., and Kuhl, E., “Use it or Lose it: Multiscale Skeletal Muscle Adaptation to Mechanical Stimuli,” Biomechanics and Modeling in Mechanobiology, Vol. 14, No. 2, pp. 195–215, 2015.

    Article  Google Scholar 

  45. Senf, S. M., Dodd, S. L., McClung, J. M., and Judge, A. R., “Hsp70 Overexpression Inhibits NF-kB and Foxo3a Transcriptional Activities and Prevents Skeletal Muscle Atrophy,” The FASEB Journal, Vol. 22, No. 11, pp. 3836–3845, 2008.

    Article  Google Scholar 

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Author notes

  1. Seohyun Kim and Donghyun Hwang contributed equally to this work

Authors and Affiliations

  1. Department of Biomedical Engineering and Research Institute for Medical Instruments & Rehabilitation Engineering, Yonsei University, 1, Yeonsedae-gil, Heungeop-myeon, Wonju-si, Gangwon-do, 26493, Republic of Korea

    Seohyun Kim, Donghyun Hwang, Hana Lee, Byungjo Jung, Jongbum Seo & Han Sung Kim

  2. Cell Biotech, 50, Aegibong-ro 409beon-gil, Gaegok-ri, Wolgot-myeon, Gimpo-si, Gyeonggi-do, 10003, Republic of Korea

    Donghyun Seo

  3. CELLOGIN, 237, Gagok-ro, Jijeong-myeon, Wonju-si, Gangwon-do, 26355, Republic of Korea

    Seungkwan Cho

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  1. Seohyun Kim
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Correspondence to Han Sung Kim.

Additional information

Seohyun Kim M.Sc. candidate in the Department of Biomedical Engineering, Yonsei University. Her research interest is Tissue Engineering.

Donghyun Hwang Ph.D. candidate in the Department of Biomedical Engineering, Yonsei University. His research interest is Tissue Engineering.

Hana Lee Ph.D. candidate in the Department of Biomedical Engineering, Yonsei University. Her research interest is Tissue Engineering.

Donghyun Seo Assistant Manager in cellbiotech research center.

Seungkwan Cho Chief Technical Officer in CELLOGIN Inc. His research interest is micro-current and multimodal stimulation for enhancing bioactivity.

Byungjo Jung Professor in the Department of Biomedical Engineering, Yonsei University. His research interest is biophotonics.

Jongbum Seo Professor in the Department of Biomedical Engineering, Yonsei University. His research interest is Biomedical Ultrasound (Therapeutic Ultrasound).

Han Sung Kim Professor in the Department of Biomedical Engineering, Yonsei University. His research interest is Computer Aided Biomedical Engineering.

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Kim, S., Hwang, D., Lee, H. et al. Therapeutic Effects of Multimodal Biophysical Stimulation on Muscle Atrophy in a Mouse Model. Int. J. Precis. Eng. Manuf. 19, 1553–1560 (2018). https://doi.org/10.1007/s12541-018-0183-z

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