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Low-Intensity Pulsed Ultrasound in Dentofacial Tissue Engineering

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Abstract

Oral and maxillofacial diseases affect millions of people worldwide and hence tissue engineering can be considered an interesting and clinically relevant approach to regenerate orofacial tissues after being affected by different diseases. Among several innovations for tissue regeneration, low-intensity pulsed ultrasound (LIPUS) has been used extensively in medicine as a therapeutic, operative, and diagnostic tool. LIPUS is accepted to promote bone fracture repair and regeneration. Furthermore, the effect of LIPUS on soft tissues regeneration has been paid much attention, and many studies have performed to evaluate the potential use of LIPUS to tissue engineering soft tissues. The present article provides an overview about the status of LIPUS stimulation as a tool to be used to enhance regeneration/tissue engineering. This review consists of five parts. Part 1 is a brief introduction of the acoustic description of LIPUS and mechanical action. In Part 2, biological problems in dentofacial tissue engineering are proposed. Part 3 explores biologic mechanisms of LIPUS to cells and tissues in living body. In Part 4, the effectiveness of LIPUS on cell metabolism and tissue regeneration in dentistry are summarized. Finally, Part 5 relates the possibility of clinical application of LIPUS in orthodontics. The present review brings out better understanding of the bioeffect of LIPUS therapy on orofacial tissues which is essential to the successful integration of management remedies for tissue regeneration/engineering. To develop an evidence-based approach to clinical management and treatment of orofacial degenerative diseases using LIPUS, we would like to be in full pursuit of LIPUS biotherapy. Still, there are many challenges for this relatively new strategy, but the up to date achievements using it promises to go far beyond the present possibilities.

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References

  1. Al-Daghreer, S., M. Doschak, A. J. Sloan, P. W. Major, G. Heo, C. Scurtescu, Y. Y. Tsui, and T. El-Bialy. Long term effect of low intensity pulsed ultrasound on a human tooth slice organ culture. Arch. Oral. Biol. 57:760–768, 2012.

    Article  PubMed  Google Scholar 

  2. Al-Daghreer, S., M. Doschak, A. J. Sloan, P. W. Major, G. Heo, C. Scurtescu, Y. Y. Tsui, and T. El-Bialy. Short-term effect of low-intensity pulsed ultrasound on an ex vivo 3-d tooth culture. Ultrasound Med. Biol. 39:1066–1074, 2013.

    Article  PubMed  Google Scholar 

  3. Al-Daghreer, S., M. R. Doschak, A. J. Sloane, P. W. Major, G. Heo, C. Scurtescu, Y. Y. Tsui, and T. El-Bialy. Effect of LIPUS on orthodontically induced root resorption in Beagle dogs. Ultrasound Med. Biol. 40:1187–1196, 2014.

    Article  PubMed  Google Scholar 

  4. Angle, S. R., K. Sena, D. R. Sumner, and A. S. Virdi. Osteogenic differentiation of rat bone marrow stromal cells by various intensities of low-intensity pulsed ultrasound. Ultrasonics 51:281–288, 2011.

    Article  CAS  PubMed  Google Scholar 

  5. Audo, R., V. Deschamps, M. Hahne, B. Combe, and J. Morel. Apoptosis is not the major death mechanism induced by celecoxib on rheumatoid arthritis synovial fibroblasts. Arthritis. Res. Ther. 9:R128, 2007.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  6. Azuma, Y., M. Ito, Y. Harada, H. Takagi, T. Ohta, and S. Jingushi. Low-intensity pulsed ultrasound accelerates rat femoral fracture healing by acting on the various cellular reactions in the fracture callus. J. Bone. Miner. Res. 16:671–680, 2001.

    Article  CAS  PubMed  Google Scholar 

  7. Bartok, B., and G. S. Firestein. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol. Rev. 233:233–255, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Bosshardt, D. D., T. Degen, and N. P. Lsng. Sequence of protein expression of bone sialoprotein and osteopontin at the developing interface between repair cementum and dentin in human deciduous teeth. Cell Tissue Res. 320:399–407, 2005.

    Article  CAS  PubMed  Google Scholar 

  9. Buckley, M. J., A. J. Banes, L. G. Levin, B. E. Sumpio, M. Sato, R. Jordan, J. Gilbert, G. W. Link, and R. Tran Son Tay. Osteoblasts increase their rate of division and align in response to cyclic mechanical tension in vitro. Bone Miner. 4:225–236, 1998.

  10. Burchardt, H., and W. F. Enneking. Transplantation of bone. Surg. Clin. N. Am. 58:403–427, 1978.

    CAS  PubMed  Google Scholar 

  11. Chapman, I. V., N. A. MacNally, and S. Tucker. Ultrasound-induced changes in rates of influx and efflux of potassium ions in rat thymocytes in vitro. Ultrasound Med. Biol. 6:47–58, 1980.

    Article  CAS  PubMed  Google Scholar 

  12. Chen, Y. J., C. J. Wang, K. D. Yang, P. R. Chang, H. C. Huang, Y. T. Huang, Y. C. Sun, and F. S. Wang. Pertussis toxin-sensitive Gαi protein and ERK dependent pathways mediate ultrasound promotion of osteogenic transcription in human osteoblasts. FEBS Lett. 554:154–158, 2003.

    Article  CAS  PubMed  Google Scholar 

  13. Claes, L., and B. Willie. The enhancement of bone regeneration by ultrasound. Prog. Biophys. Mol. Biol. 93:384–398, 2007.

    Article  PubMed  Google Scholar 

  14. Cowan, K. J., and K. B. Storey. Mitogen-activated protein kinases: new signaling pathways functioning in cellular responses to environmental stress. J. Exp. Biol. 206:1107–1115, 2003.

    Article  CAS  PubMed  Google Scholar 

  15. Dalla-Bona, D. A., E. Tanaka, H. Oka, E. Yamano, N. Kawai, M. Miyauchi, T. Takata, and K. Tanne. Effects of ultrasound on cementoblast metabolism in vitro. Ultrasound Med. Biol. 32:943–948, 2006.

    Article  PubMed  Google Scholar 

  16. Dalla-Bona, D. A., E. Tanaka, T. Inubushi, H. Oka, A. Ohta, H. Okada, M. Miyauchi, T. Takata, and K. Tanne. Cultured cementoblast stimulation by low- and high-intensity ultrasound. Arch. Oral. Biol. 53:318–323, 2008.

    Article  CAS  PubMed  Google Scholar 

  17. Delius, M., K. Draenert, Y. Al Diek, and Y. Draenert. Biological effects of shock waves: in vivo effect of high energy pulses on rabbit bone. Ultrasound. Med. Biol. 21:1219–1225, 1995.

  18. DePalma, A. F., R. H. Rothman, G. E. Lewinnek, and S. T. Canale. Anterior interbody fusion for severe cervical disc degeneration. Surg. Gynecol. Obstet. 134:755–758, 1972.

    CAS  PubMed  Google Scholar 

  19. D’Errico, J. A., H. Ouyang, J. E. Berry, R. L. MacNeil, C. Strayhorn, M. J. Imperiale, N. L. Harris, H. Goldberg, and M. J. Somerman. Immortalized cementoblasts and periodontal ligament cells in culture. Bone 25:39–47, 1999.

    Article  PubMed  Google Scholar 

  20. Dougherty, C. J., L. A. Kubasiak, H. Prentice, P. Andreka, N. H. Bishopric, and K. A. Webster. Activation of c-Jun N-terminal kinase promotes survival of cardiac myocytes after oxidative stress. Biochem. J. 362:561–571, 2002.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Duarte, L. R. The stimulation of bone growth by ultrasound. Arch. Orthop. Trauma. Surg. 101:153–159, 1983.

    Article  CAS  PubMed  Google Scholar 

  22. Dyson, M., J. B. Pond, J. Joseph, and R. Warwick. The stimulation of tissue regeneration by means of ultrasound. Clin. Sci. 35:273–285, 1968.

    CAS  PubMed  Google Scholar 

  23. Dyson, M., and M. Brookes. Stimulation of bone repair by ultrasound. Ultrasound Med. Biol. Suppl. 2:61–66, 1983.

    Google Scholar 

  24. Dyson, M. Therapeutic applications of ultrasound. In: Biological Effects of Ultrasound, edited by W. L. Nyborg, and M. C. Ziskin. New York, NY: Churchill Livingstone, 1985, pp. 121–133.

    Google Scholar 

  25. El-Bialy, T. H., T. J. Royston, R. L. Magin, C. A. Evans, A. M. Zaki, and L. A. Frizzell. The effect of pulsed ultrasound on mandibular distraction. Ann. Biomed. Eng. 30:1251–1261, 2002.

    Article  PubMed  Google Scholar 

  26. El-Bialy, T., I. El-Shamy, and T. M. Graber. Growth modification of the rabbit mandible using therapeutic ultrasound: is it possible to enhance functional appliance results? Angle Orthod. 73:631–639, 2003.

    PubMed  Google Scholar 

  27. El-Bialy, T., I. El-Shamy, and T. M. Graber. Repair of orthodontically induced root resorption by ultrasound in humans. Am. J. Orthod. Dentofacial. Orthop. 126:186–193, 2004.

    Article  PubMed  Google Scholar 

  28. El-Bialy, T. H., R. F. Elgazzar, E. E. Megahed, and T. J. Royston. Effects of ultrasound modes on mandibular osteodistraction. J. Dent. Res. 87:953–957, 2008.

    Article  CAS  PubMed  Google Scholar 

  29. El-Bialy, T., H. Uludag, N. Jomha, and S. F. Badylak. In vivo ultrasound-assisted tissue-engineered mandibular condyle: a pilot study in rabbits. Tissue Eng. Part C. Methods 16:1315–1323, 2010.

    Article  PubMed  Google Scholar 

  30. El-Bialy, T., B. Lam, S. Aldaghreer, and A. J. Sloan. The effect of low intensity pulsed ultrasound in a 3D ex vivo orthodontic model. J. Dent. 39:693–699, 2011.

    Article  CAS  PubMed  Google Scholar 

  31. El-Bialy, T., A. Alhadlaq, B. Wong, and C. Kucharski. Ultrasound effect on neural differentiation of gingival stem/progenitor cells. Ann. Biomed. Eng. 42:1406–1412, 2014.

    Article  PubMed  Google Scholar 

  32. Erdogan, O., E. Esen, Y. Ustün, M. Kürkçü, T. Akova, G. Gönlüşen, H. Uysal, and F. Cevlik. Effects of low-intensity pulsed ultrasound on healing of mandibular fractures: an experimental study in rabbits. J. Oral. Maxillofac. Surg. 64:180–188, 2006.

    Article  PubMed  Google Scholar 

  33. Faour, W. H., Y. He, Q. W. He, M. de Ladurantaye, M. Quintero, A. Mancini, and J. A. Di Battista. Prostaglandin E2 regulates the level and stability of cyclooxygenase-2 mRNA through activation of p38 mitogen-activated protein kinase in interleukin-1β-treated human synovial fibroblasts. J. Biol. Chem. 276:31720–31731, 2001.

    Article  CAS  PubMed  Google Scholar 

  34. Flower, R. J. The development of COX2 inhibitors. Nat. Rev. Drug. Dis. 2:179–191, 2003.

    Article  CAS  Google Scholar 

  35. Ghassemi-Nejad, S., T. Kobezda, T. A. Rauch, C. Matesz, T. T. Glant, and K. Mikecz. Osteoarthritis-like damage of cartilage in the temporomandibular joints in mice with autoimmune inflammatory arthritis. Osteoarthr. Cart. 19:458–465, 2011.

    Article  CAS  Google Scholar 

  36. Gu, X. Q., Y. M. Li, J. Guo, L. H. Zhang, D. Li, and X. D. Gai. Effect of low intensity pulsed ultrasound on repairing the periodontal bone of Beagle canines. Asian Pac. J. Trop. Med. 7:325–328, 2014.

    Article  PubMed  Google Scholar 

  37. Hadjiargyrou, M., K. McLeod, J. P. Ryaby, and C. Rubin. Enhancement of fracture healing by low intensity ultrasound. Clin. Orthop. Relat. Res. 355:S216–S229, 1998.

    Article  PubMed  Google Scholar 

  38. Harle, J., V. Salih, F. Mayia, J. C. Knowles, and I. Olsen. Effects of ultrasound on the growth and function of bone and periodontal ligament cells in vitro. Ultrasound Med. Biol. 27:579–586, 2001.

    Article  CAS  PubMed  Google Scholar 

  39. Hasuike, A., S. Sato, A. Udagawa, K. Ando, Y. Arai, and K. Ito. In vivo bone regenerative effect of low-intensity pulsed ultrasound in rat calvarial defects. Oral. Surg. Oral. Med. Oral. Pathol. Oral. Radiol. Endod. 111:e12–e20, 2011.

    Article  PubMed  Google Scholar 

  40. Heckman, J. D., J. P. Ryaby, J. McCabe, J. J. Frey, and R. F. Kilcoyne. Acceleration of tibial fracture-healing by non-invasive, low-intensity pulsed ultrasound. J. Bone Joint Surg. Am. 76:26–34, 1994.

    CAS  PubMed  Google Scholar 

  41. Hollender, L., A. Ronneman, and B. Thilander. Root resorption, marginal bone support and clinical crown length in orthodontically treated patients. Eur. J. Orthod. 2:197–205, 1980.

    Article  CAS  PubMed  Google Scholar 

  42. Hsu, H. C., Y. C. Fong, C. S. Chang, C. J. Hsu, S. F. Hsu, J. G. Lin, W. M. Fu, R. S. Yang, and C. H. Tang. Ultrasound induces cyclooxygenase-2 expression through integrin, integrin-linked kinase, Akt, NF-κB and p300 pathway in human chondrocytes. Cell Signal. 19:2317–2328, 2007.

    Article  CAS  PubMed  Google Scholar 

  43. Hu, B., Y. Zhang, J. Zhou, J. Li, F. Deng, Z. Wang, and J. Song. Low-intensity pulsed ultrasound stimulation facilitates osteogenic differentiation of human periodontal ligament cells. PloS One 9:e95168, 2014.

    Article  PubMed Central  PubMed  Google Scholar 

  44. Huber, L. C., O. Distler, I. Tarner, R. E. Gay, S. Gay, and T. Pap. Synovial fibroblasts: key players in rheumatoid arthritis. Rheumatology 45:669–675, 2006.

    Article  CAS  PubMed  Google Scholar 

  45. Ikai, H., T. Tamura, T. Watanabe, M. Itou, A. Sugaya, S. Iwabuchi, Y. Mikuni-Takagaki, and S. Deguchi. Low-intensity pulsed ultrasound accelerates periodontal wound healing after flap surgery. J. Periodontal. Res. 43(2):212–216, 2008.

    Article  CAS  PubMed  Google Scholar 

  46. Ikeda, E., R. Morita, K. Nakao, K. Ishida, T. Nakamura, T. Takano-Yamamoto, M. Ogawa, M. Mizuno, S. Kasuheckmangai, and T. Tsuji. Fully functional bioengineered tooth replacement as an organ replacement therapy. Proc. Natl Acad. Sci. U.S.A. 106:13475–13780, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Inubushi, T., E. Tanaka, E. B. Rego, M. Kitagawa, A. Kawazoe, A. Ohta, H. Okada, J. H. Koolstra, M. Miyauchi, T. Takata, and K. Tanne. Effects of ultrasound on the proliferation and differentiation of cementoblast lineage cells. J. Periodontol. 79:1984–1990, 2008.

    Article  CAS  PubMed  Google Scholar 

  48. Inubushi, T., E. Tanaka, E. B. Rego, J. Ohtani, A. Kawazoe, K. Tanne, M. Miyauchi, and T. Takata. Low-intensity ultrasound stimulation inhibits resorption of the tooth root induced by experimental force application. Bone 53:497–506, 2013.

    Article  PubMed  Google Scholar 

  49. Iwabuchi, Y., K. Tanimoto, Y. Tanne, T. Inubushi, T. Kamiya, Y. C. Huang, R. Kunimatsu, N. Hirose, M. Yoshioka, T. Mitsuyoshi, E. Tanaka, and K. Tanne. Effects of low-intensity pulsed ultrasound on the expression of cyclooxygenase-2 in mandibular condylar chondrocytes. J. Oral Facial Pain Headache 28:261–268, 2014.

    Article  PubMed  Google Scholar 

  50. Izumi, K., J. Song, and S. E. Feinberg. Development of a tissue-engineered human oral mucosa: from the bench to the bed side. Cells Tissues Organs 176:134–152, 2004.

    Article  PubMed  Google Scholar 

  51. Kanbe, K., K. Inoue, Y. Inoue, and Q. Chen. Inducement of mitogen-activated protein kinases in frozen shoulders. J. Orthop. Sci. 14:56–61, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. Kaur, H., H. Uludağ, and T. El-Bialy. Effect of nonviral plasmid delivered basic fibroblast growth factor and low intensity pulsed ultrasound on mandibular condylar growth: a preliminary study. Biomed. Res. Int. 2014:426710, 2014.

    PubMed Central  PubMed  Google Scholar 

  53. Kardel, R., A. K. Ulfgren, F. P. Reinholt, and A. Holmlund. Inflammatory cell and cytokine patterns in patients with painful clicking and osteoarthritis in the temporomandibular joint. Int. J. Oral. Maxillofac. Surg. 32:390–396, 2003.

    Article  CAS  PubMed  Google Scholar 

  54. Khan, Y., and C. T. Laurencin. Fracture repair with ultrasound: clinical and cell-based evaluation. J. Bone Joint Surg. Am. 90:S138–S144, 2008.

    Article  Google Scholar 

  55. Kim, S. H., and K. S. Hong. Histologic evaluation of low-intensity pulsed ultrasound effects on bone regeneration in sinus lift. J Periodontal Implant Sci. 40(6):271–275, 2010.

    Article  PubMed Central  PubMed  Google Scholar 

  56. Kokubu, T., N. Matsui, H. Fujioka, M. Tsunoda, and K. Mizuno. Low intensity pulsed ultrasound exposure increases prostaglandin E2 production via the induction of cyclooxygenase-2 mRNA in mouse osteoblasts. Biochem. Biophys. Res. Commun. 256:284–287, 1999.

    Article  CAS  PubMed  Google Scholar 

  57. Kojima, F., H. Naraba, S. Miyamoto, M. Beppu, H. Aoki, and S. Kawai. Membrane-associated prostaglandin E synthase-1 is upregulated by proinflammatory cytokines in chondrocytes from patients with osteoarthritis. Arthritis Res. Ther. 6:R355–R365, 2004.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Kubota, E., T. Kubota, J. Matsumoto, T. Shibata, and K. I. Murakami. Synovial fluid cytokines and proteinases as markers of temporomandibular joint disease. J. Oral. Maxillofac. Surg. 56:192–198, 1998.

    Article  CAS  PubMed  Google Scholar 

  59. Kurol, J., P. Owman-Moll, and D. Lundgren. Time related root resorption after application of a controlled continuous orthodontic force. Am. J. Orthod. Dentofacial. Orthop. 110:303–310, 1996.

    Article  CAS  PubMed  Google Scholar 

  60. Kyriakis, J. M., and J. Avruch. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81:807–869, 2001.

    CAS  PubMed  Google Scholar 

  61. Lal, H., S. K. Verma, M. Smith, R. S. Guleria, G. Lu, D. M. Foster, and D. E. Dostal. Stretch-induced MAP kinase activation in cardiac myocytes: differential regulation through beta 1-integrin and focal adhesion kinase. J. Mol. Cell Cardiol. 43:137–147, 2007.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  62. Iashchenko, L. V., Z. N. Ostapiak, and V. L. Semenov. The humoral mechanisms of the action of ultrasound in inflammatory lung diseases (an experimental study). Vopr. Kurortol. Fizioter. Lech. Fiz. Kult. 2:20–22, 1994.

    PubMed  Google Scholar 

  63. Leonardi, R., L. E. Almeida, and C. Loreto. Lubricin immunohistochemical expression in human temporomandibular joint disc with internal derangement. J. Oral. Pathol. Med. 40:587–592, 2011.

    Article  CAS  PubMed  Google Scholar 

  64. Levander, E., and O. Malmgren. Evaluation of the risk of root resorption during orthodontic treatment: a study of upper incisors. Eur. J. Orthod. 10:30–38, 1988.

    Article  CAS  PubMed  Google Scholar 

  65. Leung, K. S., W. H. Cheung, C. Zhang, K. M. Lee, and H. K. Lo. Low intensity pulsed ultrasound stimulates osteogenic activity of human periosteal cells. Clin. Orthop. Relat. Res. 418:253–259, 2004.

    Article  PubMed  Google Scholar 

  66. Li, F., Z. Wang, Y. Du, P. Ma, J. Bai, F. Wu, and R. Feng. Study on therapeutic dosimetry of HIFU ablation tissue. Sheng. Wu. Yi. Xue. Gong. Cheng. Xue. Za. Zhi. 23:839–843, 2006.

    PubMed  Google Scholar 

  67. Lim, K., J. Kim, H. Seonwoo, S. H. Park, P. H. Choung, and J. H. Chung. In vitro effects of low-intensity pulsed ultrasound stimulation on the osteogenic differentiation of human alveolar bone-derived mesenchymal stem cells for tooth tissue engineering. Biomed. Res. Int. 2013:269724, 2013.

    PubMed Central  PubMed  Google Scholar 

  68. Matsuda, N., K. Yokoyama, S. Takeshita, and M. Watanabe. Role of epidermal growth factor and its receptor in mechanical stress-induced differentiation of human periodontal ligament cells in vitro. Arch. Oral. Biol. 43:987–997, 1998.

    Article  CAS  PubMed  Google Scholar 

  69. Matias, M. A., H. Li, W. G. Young, and P. M. Bartold. Immunohistochemical localization of extracellular matrix proteins in the periodontium during cementogenesis in the rat molar. Arch. Oral. Biol. 48:709–716, 2003.

    Article  CAS  PubMed  Google Scholar 

  70. Mortimer, A. J., and M. Dyson. The effect of therapeutic ultrasound on calcium uptake in fibroblasts. Ultrasound Med. Biol. 14:499–506, 1988.

    Article  CAS  PubMed  Google Scholar 

  71. Mostafa, N. Z., H. Uludağ, D. N. Dederich, M. R. Doschak, and T. H. El-Bialy. Anabolic effects of low-intensity pulsed ultrasound on human gingival fibroblasts. Arch. Oral. Biol. 54:743–748, 2009.

    Article  CAS  PubMed  Google Scholar 

  72. Mukai, S., H. Ito, Y. Nakagawa, H. Akiyama, M. Miyamoto, and T. Nakamura. Transforming growth factor-β1 mediates the effects of low-intensity pulsed ultrasound in chondrocytes. Ultrasound Med. Biol. 31:1713–1721, 2005.

    Article  PubMed  Google Scholar 

  73. Nagata, K., T. Nakamura, S. Fujihara, and E. Tanaka. Ultrasound modulates the inflammatory response and promotes muscle regeneration in injured muscles. Ann. Biomed. Eng. 41:1095–1105, 2013.

    Article  PubMed  Google Scholar 

  74. Nakamura, T., S. Fujihara, T. Katsura, K. Yamamoto, T. Inubushi, K. Tanimoto, and E. Tanaka. Effects of low-intensity pulsed ultrasound on the expression and activity of hyaluronic synthase and hyaluronidase in IL-1β-stimulated synovial cells. Ann. Biomed. Eng. 38:3363–3370, 2010.

    Article  PubMed  Google Scholar 

  75. Nakamura, T., S. Fujihara, K. Yamamoto-Nagata, T. Katsura, T. Inubushi, and E. Tanaka. Low-intensity pulsed ultrasound reduces the inflammatory activity of synovitis. Ann. Biomed. Eng. 39:2964–2971, 2011.

    Article  PubMed  Google Scholar 

  76. Nakashima, M., K. Tachibana, K. Iohara, M. Ito, M. Ishikawa, and A. Akamine. Induction of reparative dentin formation by ultrasound-mediated gene delivery of growth/differentiation factor 11. Hum. Gene. Ther. 14:591–597, 2003.

    Article  CAS  PubMed  Google Scholar 

  77. Naruse, K., Y. Mikuni-Takagaki, Y. Azuma, M. Ito, T. Oota, K. Kameyama, and M. Itoman. Anabolic response of mouse bone-marrow-derived stromal cell clone ST2 cells to low-intensity pulsed ultrasound. Biochem. Biophys. Res. Commun. 268:216–220, 2000.

    Article  CAS  PubMed  Google Scholar 

  78. Naruse, K., A. Miyauchi, M. Itoman, and Y. Mikuni-Takagaki. Distinct anabolic response of osteoblasts to low-intensity pulsed ultrasound. J. Bone. Miner. Res. 18:360–369, 2003.

    Article  CAS  PubMed  Google Scholar 

  79. Neumann, E., S. Lefèvre, B. Zimmermann, S. Gay, and U. Müller-Ladner. Rheumatoid arthritis progression mediated by activated synovial fibroblasts. Trends. Mol. Med. 16:458–468, 2010.

    Article  CAS  PubMed  Google Scholar 

  80. Norvell, S. M., M. Alvarez, J. P. Bidwell, and F. M. Pavalko. Fluid shear stress induces beta-catenin signaling in osteoblasts. Calcif. Tissue. Int. 75:396–404, 2004.

    Article  CAS  PubMed  Google Scholar 

  81. Oyonarte, R., M. Zárate, and F. Rodriguez. Low-intensity pulsed ultrasound stimulation of condylar growth in rats. Angle Orthod. 79:964–970, 2009.

    Article  PubMed  Google Scholar 

  82. Oyonarte, R., D. Becerra, J. Díaz-Zúñiga, V. Rojas, and F. Carrion. Morphological effects of mesenchymal stem cells and pulsed ultrasound on condylar growth in rats: a pilot study. Aust. Orthod. J. 29:3–12, 2013.

    PubMed  Google Scholar 

  83. Padilla, F., R. Puts, L. Vico, and K. Raum. Stimulation of bone repair with ultrasound: a review of the possible mechanic effects. Ultrasounics 54:1125–1145, 2014.

    Article  CAS  Google Scholar 

  84. Pavlin, D., and J. Gluhak-Heinrich. Effect of mechanical loading on periodontal cells. Crit. Rev. Oral. Biol. Med. 12:414–424, 2001.

    Article  CAS  PubMed  Google Scholar 

  85. Pilla, A. A., M. A. Mont, P. R. Nasser, S. A. Khan, M. Figueiredo, J. J. Kaufman, and R. S. Siffert. Non-invasive low-intensity pulsed ultrasound accelerates bone healing in the rabbit. J. Orthop. Trauma. 4:246–253, 1990.

    Article  CAS  PubMed  Google Scholar 

  86. Rees, L. A. The structure and function of the mandibular joint. Brit. Dent. J. 96:125–133, 1954.

    Google Scholar 

  87. Rego, E. B., T. Inubushi, A. Kawazoe, K. Tanimoto, M. Miyauchi, E. Tanaka, T. Takata, and K. Tanne. Ultrasound stimulation induces PGE2 synthesis promoting cementoblastic differentiation through EP2/EP4 receptor pathway. Ultrasound. Med. Biol. 36:907–915, 2010.

    Article  PubMed  Google Scholar 

  88. Rego, E. B., T. Inubushi, M. Miyauchi, A. Kawazoe, E. Tanaka, T. Takata, and K. Tanne. Ultrasound stimulation attenuates root resorption on rat replanted molars and impairs TNF-α signaling in vitro. J. Periodont. Res. 46:648–654, 2011.

    Article  CAS  PubMed  Google Scholar 

  89. Ren, L., Z. Yang, J. Song, Z. Wang, F. Deng, and W. Li. Involvement of p38 MAPK pathway in low intensity pulsed ultrasound induced osteogenic differentiation of human periodontal ligament cells. Ultrasonics 53(3):686–690, 2013. doi:10.1016/j.ultras.2012.10.008.

    Article  CAS  PubMed  Google Scholar 

  90. Rita, F. N., E. W. David, and L. G. James. Tooth resorption. Quint. Int. 30:9–25, 1999.

    Google Scholar 

  91. Ritchie, R., J. Collin, C. Coussios, and T. Leslie. Attenuation and de-focusing during high-intensity focused ultrasound therapy through peri-nephric fat. Ultrasound. Med. Biol. 39:1785–1793, 2013.

    Article  PubMed  Google Scholar 

  92. Romano, C. L., D. Romano, and N. Logoluso. Low-intensity pulsed ultrasound for the treatment of bone delayed union or nonunion: a review. Ultrasound. Med. Biol. 35:529–536, 2009.

    Article  PubMed  Google Scholar 

  93. Saito, M., K. Fujii, T. Tanaka, and S. Soshi. Effect of low and high intensity pulsed ultrasound on collagen post-translational modifications in MC3T3-E1 osteoblasts. Calcif. Tissue Int. 75:384–395, 2004.

    Article  CAS  PubMed  Google Scholar 

  94. Sameshima, G. T., and P. M. Sinclair. Predicting and preventing root resorption: part II. Treatment factors. Am. J. Orthod. Dentofacial. Orthop. 119:511–515, 2001.

  95. Sato, M., K. Nagata, S. Kuroda, S. Horiuchi, K. Mansjur, T. Nakamura, T. Inubushi, and E. Tanaka. Low-intensity pulsed ultrasound activates integrin-mediated mechanotransduction pathway in synovial cells. Ann. Biomed. Eng. 40:2156–2163, 2014.

    Article  Google Scholar 

  96. Scheven, B. A., J. Man, J. L. Millard, P. R. Cooper, S. C. Lea, A. D. Walmsley, and A. J. Smith. VEGF and odontoblast-like cells: stimulation by low frequency ultrasound. Arch. Oral. Biol. 54:185–191, 2009.

    Article  CAS  PubMed  Google Scholar 

  97. Schumann, D., R. Kujat, J. Zellner, M. K. Angele, M. Nerlich, E. Mayr, and P. Angele. Treatment of human mesenchymal stem cells with pulsed low intensity ultrasound enhances the chondrogenic phenotype in vitro. Biorheology 43:431–443, 2006.

    CAS  PubMed  Google Scholar 

  98. Scott, D. L., F. Wolfe, and T. W. Huizinga. Rheumatoid arthritis. Lancet 376:1094–1108, 2010.

    Article  PubMed  Google Scholar 

  99. Sellam, J., and F. Berenbaum. The role of synovitis in pathophysiology and clinical symptoms of osteoarthritis. Nat. Rev. Rheum. 6:625–635, 2010.

    Article  CAS  Google Scholar 

  100. Shiraishi, R., C. Masaki, A. Toshinaga, T. Okinaga, T. Nishihara, N. Yamanaka, T. Nakamoto, and R. Hosokawa. The effects of low-intensity pulsed ultrasound exposure on gingival cells. J Periodontol. 82(10):1498–1503, 2011.

    Article  CAS  PubMed  Google Scholar 

  101. Skutek, M., M. van Griensven, J. Zeichen, N. Brauer, and U. Bosch. Cyclic mechanical stretching of human patellar tendon fibroblasts: activation of JNK and modulation of apoptosis. Knee Surg. Sports Traumatol. Arthroscopy 11:122–129, 2003.

    Google Scholar 

  102. Summer, W., and M. K. Patrick. Ultrasonic Therapy. Amsterdam: Elsevier Pub. Co, pp. 63–68, 1964.

    Google Scholar 

  103. Takayama, T., N. Suzuki, K. Ikeda, T. Shimada, A. Suzuki, M. Maeno, K. Otsuka, and K. Ito. Low-intensity pulsed ultrasound stimulates osteogenic differentiation in ROS 17/2.8 cells. Life. Sci. 80:965–971, 2007.

  104. Takeuchi, R., A. Ryo, N. Komitsu, Y. Mikuni-Takagaki, A. Fukui, Y. Takagi, T. Shiraishi, S. Morishita, Y. Yamazaki, K. Kumagai, I. Aoki, and T. Saito. Low-intensity pulsed ultrasound activates the phosphatidylinositol 3 kinase/Akt pathway and stimulates the growth of chondrocytes in three-dimensional cultures: a basic science study. Arthritis. Res. Ther. 10:R77, 2008.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  105. Tanaka, E., J. Aoyama, M. Miyauchi, T. Takata, K. Hanaoka, T. Iwabe, and K. Tanne. Vascular endothelial growth factor plays an important autocrine/paracrine role in the progression of osteoarthritis. Histochem. Cell Biol. 123:275–281, 2005.

    Article  CAS  PubMed  Google Scholar 

  106. Tang, C. H., R. S. Yang, T. H. Huang, D. Y. Lu, W. J. Chuang, T. F. Huang, and W. M. Fu. Ultrasound stimulates cyclooxygenase-2 expression and increases bone formation through integrin, focal adhesion kinase, phosphatidylinositol 3-kinase, and Akt pathway in osteoblasts. Mol. Pharmacol. 69:2047–2057, 2006.

    Article  CAS  PubMed  Google Scholar 

  107. Ten Cate, A. R. The periodontium: Oral histology, development, structure and function. St Louis, MO: Mosby, pp. 276–279, 2003.

    Google Scholar 

  108. Trope, M. Regenerative potential of dental pulp. J. Endod. 34:S13–S17, 2008.

    Article  PubMed  Google Scholar 

  109. Tsai, C. L., W. H. Chang, and T. K. Liu. Preliminary studies of duration and intensity of ultrasonic treatments on fracture repair. Chin. J. Physiol. 35:21–26, 1992.

    CAS  PubMed  Google Scholar 

  110. Vafaeian, B., M. El-Rich, T. El-Bialy, and S. Adeeb. The finite element method for micro-scale modeling of ultrasound propagation in cancellous bone. Ultrasonics 54:1663–1676, 2014.

    Article  CAS  PubMed  Google Scholar 

  111. Wang, Y., Z. Chai, Y. Zhang, F. Deng, Z. Wang, and J. Song. Influence of low-intensity pulsed ultrasound on osteogenic tissue regeneration in a periodontal injury model: X-ray image alterations assessed by micro-computed tomography. Ultrasonics 54(6):1581–1584, 2014. doi:10.1016/j.ultras.2014.03.015. Epub 2014 Apr 18.

  112. Warden, S. J., K. L. Bennell, J. M. McMeeken, and J. D. Wark. Acceleration of fresh fracture repair using the sonic accelerated fracture healing system (SAFHS): a review. Calcif. Tissue. Int. 66:157–163, 2000.

    Article  CAS  PubMed  Google Scholar 

  113. Warden, S. J., J. M. Favaloro, K. L. Bennell, J. M. McMeeken, K. W. Ng, J. D. Zajac, and J. D. Wark. Low-intensity pulsed ultrasound stimulates a bone forming response in UMR-106 cells. Biochem. Biophys. Res. Commun. 286:443–450, 2001.

    Article  CAS  PubMed  Google Scholar 

  114. Warwick, R., and P. L. Williams. Gray’s Anatomy. Philadelphia, PA: Saunders Co., 1973.

    Google Scholar 

  115. Widegren, U., C. Wretman, A. Lionikas, G. Hedin, and J. Henriksson. Influence of exercise intensity on ERK/MAP kinase signalling in human skeletal muscle. Pflug. Arch. 441:317–322, 2000.

    Article  CAS  Google Scholar 

  116. Yang, R. S., W. L. Lin, Y. Z. Chen, C. H. Tang, T. H. Huang, B. Y. Lu, and W. M. Fu. Regulation by ultrasound treatment on the integrin expression and differentiation of osteoblasts. Bone 36:276–283, 2005.

    Article  CAS  PubMed  Google Scholar 

  117. Yoshida, H., S. Fujita, M. Nishida, and T. Iizuka. Immunohistochemical distribution of lymph capillaries and blood capillaries in the synovial membrane in cases of internal derangement of the temporomandibular joint. J. Oral. Pathol. Med. 26:356–361, 1997.

    Article  CAS  PubMed  Google Scholar 

  118. Yoon, J. H., E. Y. Roh, S. Shin, N. H. Jung, E. Y. Song, D. S. Lee, K. S. Han, J. S. Kim, B. J. Kim, H. W. Jeon, and K. S. Yoon. Introducing pulsed low-intensity ultrasound to culturing human umbilical cord-derived mesenchymal stem cells. Biotechnol. Lett. 31:329–335, 2009.

    Article  CAS  PubMed  Google Scholar 

  119. Young, S. R., and M. Dyson. The effect of therapeutic ultrasound on angiogenesis. Ultrasound Med. Biol. 16:261–269, 1990.

    Article  CAS  PubMed  Google Scholar 

  120. Young, S. R., R. Gerard-O’Riley, J. B. Kim, and F. M. Pavalko. Focal adhesion kinase is important for fluid shear stress-induced mechanotransduction in osteoblasts. J. Bone. Miner. Res. 24:411–424, 2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  121. Zhou, S., A. Schmelz, T. Seufferlein, Y. Li, J. Zhao, and M. G. Bachem. Molecular mechanisms of low intensity pulsed ultrasound in human skin fibroblasts. J. Biol. Chem. 279:54463–54469, 2004.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Orthodontics and Dentofacial Orthopedics, Institute of Health Biosciences, Tokushima University Graduate School, 3-18-15 Kuramoto-cho, Tokushima, 770-8504, Japan

    Eiji Tanaka, Shingo Kuroda & Shinya Horiuchi

  2. ITO Co., LTD, Tokyo, Japan

    Akira Tabata

  3. Division of Orthodontics, School of Dentistry, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, AB, Canada

    Tarek El-Bialy

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  1. Eiji Tanaka
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  2. Shingo Kuroda
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  3. Shinya Horiuchi
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Correspondence to Eiji Tanaka.

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Associate Editor Daniel Elson oversaw the review of this article.

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Tanaka, E., Kuroda, S., Horiuchi, S. et al. Low-Intensity Pulsed Ultrasound in Dentofacial Tissue Engineering. Ann Biomed Eng 43, 871–886 (2015). https://doi.org/10.1007/s10439-015-1274-y

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