Therapeutic ultrasound induces periosteal ossification without apparent changes in cartilage

Connective Tissue Research

Volumn 50, Issue 1, 2009, Pages 55-63

  Naruse, Kouji ^a   Mikuni Takagaki, Yuko ^b   Urabe, Ken ^a   Uchida, Kentaroo ^c   Itoman, Moritoshi ^a  

^a KITASATO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KANAGAWA DENTAL COLLEGE   (Japan)

^c KITASATO UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

Author keywords

Cartilage; Low Intensity Pulsed Ultrasound; Organ culture; Osteogenesis; Periosteum

Indexed keywords

ALIZARIN RED S; OSTEOCALCIN; PROTEOGLYCAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE CELL; BONE DEVELOPMENT; BONE GROWTH; CALCIFICATION; CARTILAGE CELL; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; CULTURE MEDIUM; ENCHONDRAL OSSIFICATION; EPIPHYSEAL CARTILAGE; FEMUR; HISTOCHEMISTRY; IMMOBILIZATION; IMMUNOHISTOCHEMISTRY; MINERALIZATION; MORPHOLOGY; NEWBORN; NONHUMAN; ORGAN CULTURE; OSSIFICATION; PERIOSTEUM; PROTEIN SECRETION; RAT; THREE DIMENSIONAL IMAGING; TISSUE CULTURE; ULTRASOUND;

ANIMALS; BODY WEIGHTS AND MEASURES; CARTILAGE; CHONDROITIN SULFATES; FEMUR; HISTOCYTOCHEMISTRY; HYALURONIC ACID; OSTEOGENESIS; PERIOSTEUM; RATS; RATS, WISTAR; TOMOGRAPHY, X-RAY COMPUTED; ULTRASONIC THERAPY;

RATTUS;

EID: 60549087173     PISSN: 03008207     EISSN: 16078438     Source Type: Journal    
DOI: 10.1080/03008200802419855     Document Type: Article

References (42)

1. Hadjiargyrou, M., McLeod, K., Ryaby, J. P. and Rubin, C. (1998) Enhancement of fracture healing by low intensity ultrasound. Clin. Orthop., pp. S216-S229.
2. Rubin, C., Bolander, M., Ryaby, J. P. and Hadjiargyrou, M. (2001) The use of low-intensity ultrasound to accelerate the healing of fractures. J. Bone Joint Surg. Am., 83, pp. 259-270.
3. Warden, S. J., Bennell, K. L., McMeeken, J. M. and Wark, J. D. (2000) Acceleration of fresh fracture repair using the sonic accelerated fracture healing system (SAFHS): A review. Calcif. Tissue Int., 66, pp. 157-163.
4. Naruse, K., Miyauchi, A., Itoman, M. and Mikuni-Takagaki, Y. (2003) Distinct response of osteoblast to low-intensity pulsed ultrasound. J. Bone Miner. Res., 18, pp. 360-369.
5. Kokubu, T., Matsui, N., Fujioka, H., Tsunoda, M. and Mizuno, K. (1999) Low intensity pulsed ultrasound exposure increases prostaglandin E2 production via the induction of cyclooxygenase-2 mRNA in mouse osteoblasts. Biochem. Biophys. Res. Commun., 256, pp. 284-287.
6. Naruse, K., Mikuni-Takagaki, Y., Azuma, Y., Ito, M., Oota, T., Kameyama, K. and Itoman, M. (2000) Anabolic response of mouse bone-marrow-derived stromal cell clone ST2 cells to low-intensity pulsed ultrasound. Biochem. Biophys. Res. Commun., 268, pp. 216-220.
7. Warden, S. J., Favaloro, J. M., Bennell, K. L., McMeeken, J. M., Ng, K. W., Zajac, J. D. and Wark, J. D. (2001) Low-intensity pulsed ultrasound stimulates a bone-forming response in UMR-106 cells. Biochem. Biophys. Res. Commun., 286, pp. 443-450.
8. Keila, S., Kelner, A. and Weinreb, M. (2001) Systemic prostaglandin E2 increases cancellous bone formation and mass in aging rats and stimulates their bone marrow osteogenic capacity in vivo and in vitro. J. Endocrinol., 168, pp. 131-139.
9. Miyamoto, K., Suzuki, H., Yamamoto, S., Saitoh, Y., Ochiai, E., Moritani, S., Yokogawa, K., Waki, Y., Kasugai, S., Sawanishi, H. and Yamagami, H. (2003) Prostaglandin E2-mediated anabolic effect of a novel inhibitor of phosphodiesterase 4, XT-611, in the in vitro bone marrow culture. J. Bone Miner. Res., 18, pp. 1471-1477.
10. Kawaguchi, H., Pilbeam, C. C., Harrison, J. R. and Raisz, L. G. (1995) The role of prostaglandins in the regulation of bone metabolism. Clin. Orthop., 313, pp. 36-46.
11. Pilbeam, C. C., Raisz, L. G., Voznesensky, O., Alander, C. B., Delman, B. N. and Kawaguchi, H. (1995) Autoregulation of inducible prostaglandin G/H synthase in osteoblastic cells by prostaglandins. J. Bone Miner. Res., 10, pp. 406-414.
12. Miyauchi, A., Notoya, K., Mikuni-Takagaki, Y., Takagi, Y., Goto, M., Miki, Y., Takano-Yamamoto, T., Fujii, Y., Jinnai, K., Takahashi, K., Kumegawa, M., Chihara, K. and Fujita, T. (2000) Parathyroid hormone-activated volume sensitive calcium influx pathways in mechanically loaded osteocytes. J. Biol. Chem., 275, pp. 3335-3342.
13. Ryder, K. D. and Duncan, R. L. (2001) Parathyroid hormone enhances fluid shear-induced [Ca2+]i signaling in osteoblastic cells through activation of mechanosensitive and voltage-sensitive Ca2+ channels. J. Bone. Miner. Res., 16, pp. 240-248.
14. Neidlinger-Wilke, C., Stalla, I., Claes, L., Brand, R., Hoellen, I., Rubenacker, S., Arand, M. and Kinzl, L. (1995) Human osteoblasts from younger normal and osteoporotic donors show differences in proliferation and TGF beta-release in response to cyclic strain. J. Biomech., 28, pp. 1411-1418.
15. Cheng, M., Zaman, G., Rawlinson, S. C., Mohan, S., Baylink, D. J. and Lanyon, L. E. (1999) Mechanical strain stimulates ROS cell proliferation through IGF-II and estrogen through IGF-I. J. Bone Miner. Res., 14, pp. 1742-1750.
16. Li, G., Berven, S., Simpson, H. and Triffitt, J. T. (1998) Expression of BMP-4 mRNA during distraction osteogenesis in rabbits. Acta Orthop. Scand., 69, pp. 420-425.
17. Ikegame, M., Ishibashi, O., Yoshizawa, T., Shimomura, J., Komori, T., Ozawa, H. and Kawashima, H. (2001) Tensile stress induces bone morphogenetic protein 4 in preosteoblastic and fibroblastic cells, which later differentiate into osteoblasts leading to osteogenesis in the mouse calvariae in organ culture. J. Bone Miner. Res., 16, pp. 24-32.
18. Mikuni-Takagaki, Y., Naruse, K. and Azuma, Y. (2001) The role of calcium channels in osteocyte function. J. Musculoskel. Neuron. Interact., 2, pp. 255-258.
19. Azuma, Y., Ito, M., Harada, Y., Takagi, H., Ohta, T. and Jingushi, S. (2001) 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, pp. 671-680.
20. Nishikori, T., Ochi, M., Uchio, Y., Maniwa, S., Kataoka, H., Kawasaki, K., Katsube, K. and Kuriwaka, M. (2002) Effects of low-intensity pulsed ultrasound on proliferation and chondroitin sulfate synthesis of cultured chondrocytes embedded in Atelocollagen gel. J. Biomed. Mater. Res., 59, pp. 201-206.
21. Parvizi, J., Parpura, V., Greenleaf, J. F. and Bolander, M. E. (2002) Calcium signaling is required for ultrasound-stimulated aggrecan synthesis by rat chondrocytes. J. Orthop. Res., 20, pp. 51-57.
22. Zhang, Z. J., Huckle, J., Francomano, C. A. and Spencer, RG. (2003) The effects of pulsed low-intensity ultrasound on chondrocyte viability, proliferation, gene expression and matrix production. Ultrasound Med. Biol., 29, pp. 1645-1651.
23. Ogurtan, Z., Celik, I., Izci, C., Boydak, M., Alkan, F. and Yilmaz, K. (2002) Effect of experimental therapeutic ultrasound on the distal antebrachial growth plates in one-month-old rabbits. Vet. J., 164, pp. 280-287.
24. Rawool, N. M., Goldberg, B. B., Forsberg, F., Winder, A. A. and Hume, E. (2003) Power Doppler assessment of vascular changes during fracture treatment with low-intensity ultrasound. J. Ultrasound Med., 22, pp. 145-153.
25. Reuter, U., Strempel, F., John, F. and Knoch, H. G. (1984) Modification of bone fracture healing by ultrasound in an animal experiment model. Z. Exp. Chir. Transplant. Kunstliche Organe, 17, pp. 290-297.
26. Cook, S. D., Ryaby, J. P., McCabe, J., Frey, J. J., Heckman, J. D. and Kristiansen, T. K. (1997) Acceleration of tibia and distal radius fracture healing in patients who smoke. Clin. Orthop., 337, pp. 198-207.
27. Ito, M., Azuma, Y. and Harada, Y. (1998) Low intenslty pulsed ultrasound accelerates fracture healing in a rat femoral fracture model. Trans. Orthop. Res. Soc., 23, p. 732.
28. Reher, P., Doan, N., Bradnock, B., Meghji, S. and Harris, M. (1999) Effect of ultrasound on the production of IL-8, basic FGF and VEGF. Cytokine, 11, pp. 416-423.
29. Lee, G. J., Evans, J. E., Tieckelmann, H., Dulaney, J. T. and Naylor, E. W. (1980) Enzymatic studies of urinary isomeric chondroitin sulfates from patients with mucopolysaccharidoses. The application of high performance liquid chromatography. Clin. Chim. Acta, 104, pp. 65-75.
30. Leung, K. S., Cheung, W. H., Zhang, C., Lee, K. M. and Lo, H. K. (2004) Low intensity pulsed ultrasound stimulates osteogenic activity of human periosteal cells. Clin. Orthop, pp. 253-259.
31. Wiltink, A., Nijweide, P. J., Oosterbaan, W. A., Hekkenberg, R. T. and Helders, P. J. (1995) Effect of therapeutic ultrasound on endochondral ossification. Ultrasound Med. Biol., 21, pp. 121-127.
32. Nolte, P. A., Klein-Nulend, J., Albers, G. H., Marti, R. K., Semeins, C. M., Goei, S. W. and Burger, E. H. (2001) Low-intensity ultrasound stimulates endochondral ossification in vitro. J. Orthop. Res., 19, pp. 301-307.
33. Korstjens, C. M., Nolte, P. A., Burger, E. H., Albers, G. H., Semeins, C. M., Aartman, I. H., Goei, S. W. and Klein-Nulend, J. (2004) Stimulation of bone cell differentiation by low-intensity ultrasound-Histomorphometric in vitro study. J. Orthop. Res., 22, pp. 495-500.
34. Lyon, R., Liu, X. C. and Meier, J. (2003) The effects of therapeutic vs. high-intensity ultrasound on the rabbit growth plate. J. Orthop. Res., 21, pp. 865-871.
35. Nelson, F. R., Brighton, C. T., Ryaby, J., Simon, B. J., Nielson, J. H., Lorich, D. G., Bolander, M. and Seelig, J. (2003) Use of physical forces in bone healing. J. Am. Acad. Orthop. Surg., 11, pp. 344-354.
36. Yang, K. H., Parvizi, J., Wang, S. J., Lewallen, D. G., Kinnick, R. R., Greenleaf, J. F. and Bolander, M. E. (1996) Exposure to low-intensity ultrasound increases aggrecan gene expression in a rat femur fracture model. J. Orthop. Res., 14, pp. 802-809.
37. Wakita, R., Izumi, T. and Itoman, M. (1998) Thyroid hormone-induced chondrocyte terminal differentiation in rat femur organ culture. Cell Tissue Res., 293, pp. 357-364.
38. Ghilzon, R., McCulloch, C. A. and Zohar, R. (1999) Stromal mesenchymal progenitor cells. Leuk. Lymphoma, 32, pp. 211-221.
39. Schantz, J. T., Hutmacher, D. W., Chim, H., Ng, K. W., Lim, T. C. and Teoh, S. H. (2002) Induction of ectopic bone formation by using human periosteal cells in combination with a novel scaffold technology. Cell Transplant., 11, pp. 125-138.
40. Wakitani, S., Goto, T., Pineda, S. J., Young, R. G., Mansour, J. M., Caplan, A. I. and Goldberg, V. M. (1994) Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J. Bone Joint Surg. Am., 76, pp. 579-592.
41. Zohar, R., Sodek, J. and McCulloch, C. A. (1997) Characterization of stromal progenitor cells enriched by flow cytometry. Blood, 90, pp. 3471-3481.
42. Naruse, K., Urabe, K., Mukaida, T., Ueno, T., Migishima, F., Oikawa, A., Mikuni-Takagaki, Y. and Itoman, M. (2004) Spontaneous differentiation of mesenchymal stem cells obtained from fetal rat circulation. Bone, 35, pp. 850-858.