Ultrasound in Medicine and Biology
Volume 35, Issue 7 , Pages 1109-1118 , July 2009

Shockwave Exerts Osteogenic Effect on Osteoporotic Bone In an Ovariectomized Goat Model

  • Kam-Fai Tam, PhD

      Affiliations

    • Department of Orthopaedics and Traumatology, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China
    • Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China
  • ,
  • Wing-Hoi Cheung, PhD

      Affiliations

    • Department of Orthopaedics and Traumatology, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China
  • ,
  • Kwong-Man Lee, PhD

      Affiliations

    • Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China
  • ,
  • Ling Qin, PhD

      Affiliations

    • Department of Orthopaedics and Traumatology, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China
  • ,
  • Kwok-Sui Leung, MD

      Affiliations

    • Department of Orthopaedics and Traumatology, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China
    • Corresponding Author InformationAddress correspondence to: Kwok-Sui Leung, MD, Department of Orthopaedics and Traumatology, Prince of Wales Hospital, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong.

Received 14 July 2008 ,Revised 18 December 2008 ,Accepted 3 January 2009.

References 

  1. Augat P, Claes L, Suger G. In vivo effect of shock-waves on the healing of fractured bone. Clin Biomech (Bristol, Avon). 1995;10:374–378
  2. Birnbaum K, Wirtz DC, Siebert CH, Heller KD. Use of extracorporeal shock-wave therapy (ESWT) in the treatment of non-unions. A review of the literature. Arch Orthop Trauma Surg. 2002;122:324–330
  3. Chen HS, Chen LM, Huang TW. Treatment of painful heel syndrome with shock waves. Clin Orthop Relat Res. 2001;387:41–46
  4. Cummings SR, Black DM, Nevitt MC, Browner W, Cauley J, Ensrud K, et al. Bone density at various sites for prediction of hip fractures. The Study of Osteoporotic Fractures Research Group. Lancet. 1993;341:72–75
  5. Dambacher MA, Neff M, Kissling R, Qin L. Highly precise peripheral quantitative computed tomography for the evaluation of bone density, loss of bone density and structures. Consequences for prophylaxis and treatment. Drugs Aging. 1998;12:S15–S24
  6. Delius M, Draenert K, Al Diek Y, Draenert Y. Biological effects of shock waves: In vivo effect of high energy pulses on rabbit bone. Ultrasound Med Biol. 1995;21:1219–1225
  7. Eyres KS, Saleh M, Kanis JA. Effect of pulsed electromagnetic fields on bone formation and bone loss during limb lengthening. Bone. 1996;18:505–509
  8. Haake M, Boddeker IR, Decker T, Buch M, Vogel M, Labek G, et al. Side-effects of extracorporeal shock wave therapy (ESWT) in the treatment of tennis elbow. Arch Orthop Trauma Surg. 2002;122:222–228
  9. Heckman JD, Ryaby JP, McCabe J, Frey JJ, Kilcoyne RF. Acceleration of tibial fracture-healing by non-invasive, low-intensity pulsed ultrasound. J Bone Joint Surg Am. 1994;76:26–34
  10. Hildebrand T, Laib A, Muller R, Dequeker J, Ruegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: Microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res. 1999;14:1167–1174
  11. Hornby SB, Ford SL, Mase CA, Evans GP. Skeletal changes in the ovariectomised ewe and subsequent response to treatment with 17 beta oestradiol. Bone. 1995;17:S389–S394
  12. Ito M, Nishida A, Kono J, Kono M, Uetani M, Hayashi K. Which bone densitometry and which skeletal site are clinically useful for monitoring bone mass?. Osteoporos Int. 2003;14:959–964
  13. Jerome CP, Johnson CS, Vafai HT, Kaplan KC, Bailey J, Capwell B, et al. Effect of treatment for 6 months with human parathyroid hormone (1-34) peptide in ovariectomized cynomolgus monkeys (Macaca fascicularis). Bone. 1999;25:301–309
  14. Jiang Y, Zhao J, Geusens P, Liao EY, Adriaensens P, Gelan J, et al. Femoral neck trabecular microstructure in ovariectomized ewes treated with calcitonin: MRI microscopic evaluation. J Bone Miner Res. 2005;20:125–130
  15. Johannes EJ, Kaulesar Sukul DM, Matura E. High-energy shock waves for the treatment of nonunions: An experiment on dogs. J Surg Res. 1994;57:246–252
  16. Kaulesar Sukul DM, Johannes EJ, Pierik EG, van Eijck GJ, Kristelijn MJ. The effect of high energy shock waves focused on cortical bone: An in vitro study. J Surg Res. 1993;54:46–51
  17. Leung KS, Siu WS, Cheung NM, Lui PY, Chow DH, James A, et al. Goats as an osteopenic animal model. J Bone Miner Res. 2001;16:2348–2355
  18. Leung KS, Lee KM, Cheung WH, Ng ES, Qin L. Characteristics of long bone DXA reference data in Hong Kong Chinese. J Clin Densitom. 2004;7:192–200
  19. Leung KS, Lee WS, Cheung WH, Qin L. Lack of efficacy of low-intensity pulsed ultrasound on prevention of postmenopausal bone loss evaluated at the distal radius in older Chinese women. Clin Orthop Relat Res. 2004;427:234–240
  20. Leung KS, Lee WS, Tsui HF, Liu PP, Cheung WH. Complex tibial fracture outcomes following treatment with low-intensity pulsed ultrasound. Ultrasound Med Biol. 2004;30:389–395
  21. Leung KS, Siu WS, Li SF, Qin L, Cheung WH, Tam KF, et al. An in vitro optimized injectable calcium phosphate cement for augmenting screw fixation in osteopenic goats. J Biomed Mater Res B Appl Biomater. 2006;78:153–160
  22. Lu H, Qin L, Fok P, Cheung W, Lee K, Guo X, et al. Low-intensity pulsed ultrasound accelerates bone-tendon junction healing: A partial patellectomy model in rabbits. Am J Sports Med. 2006;34:1287–1296
  23. Maier M, Milz S, Tischer T, Munzing W, Manthey N, Stabler A, et al. Influence of extracorporeal shock-wave application on normal bone in an animal model in vivo. Scintigraphy, MRI and histopathology. J Bone Joint Surg (Br). 2002;84:592–599
  24. Martini L, Giavaresi G, Fini M, Torricelli P, de Pretto M, Schaden W, et al. Effect of extracorporeal shock wave therapy on osteoblastlike cells. Clin Orthop Relat Res. 2003;269–280
  25. McClure SR, Van Sickle D, White MR. Effects of extracorporeal shock wave therapy on bone. Vet Surg. 2004;33:40–48
  26. Melton LJ, Atkinson EJ, O'Fallon WM, Wahner HW, Riggs BL. Long-term fracture prediction by bone mineral assessed at different skeletal sites. J Bone Miner Res. 1993;8:1227–1233
  27. Meunier PJ, Vignot E, Garnero P, Confavreux E, Paris E, Liu-Leage S, et al. Treatment of postmenopausal women with osteoporosis or low bone density with raloxifene. Raloxifene Study Group. Osteoporos Int. 1999;10:330–336
  28. Miller DL, Thomas RM. The role of cavitation in the induction of cellular DNA damage by ultrasound and lithotripter shock waves in vitro. Ultrasound Med Biol. 1996;22:681–687
  29. Mishima S. The effect of long-term pulsing electromagnetic field stimulation on experimental osteoporosis of rats. J UOEH. 1988;10:31–45
  30. Narasaki K, Shimizu H, Beppu M, Aoki H, Takagi M, Takashi M. Effect of extracorporeal shock waves on callus formation during bone lengthening. J Orthop Sci. 2003;8:474–481
  31. Nolte PA, van der Krans A, Patka P, Janssen IM, Ryaby JP, Albers GH. Low-intensity pulsed ultrasound in the treatment of nonunions. J Trauma. 2001;51:693–702discussion 702–703
  32. North American Menopause Society . Management of postmenopausal osteoporosis: position statement of the North American Menopause Society. Menopause. 2002;9:84–101
  33. Oden ZM, Selvitelli DM, Bouxsein ML. Effect of local density changes on the failure load of the proximal femur. J Orthop Res. 1999;17:661–667
  34. Ogden JA, Toth-Kischkat A, Schultheiss R. Principles of shock wave therapy. Clin Orthop Relat Res. 2001;8–17
  35. O'Leary JM, Knothe Tate ML, Knothe U. Extracorporeal shock waves generate new bone in skeletally mature rats. Trans ORS. 2006;344
  36. Passi N, Gefen A. Trabecular bone contributes to strength of the proximal femur under mediolateral impact in the avian. J Biomech Eng. 2005;127:198–203
  37. Qin L, Mak AT, Cheng CW, Hung LK, Chan KM. Histomorphological study on pattern of fluid movement in cortical bone in goats. Anat Rec. 1999;255:380–387
  38. Qin L, Au SK, Chan KM, Lau MC, Woo J, Dambacher MA, et al. Peripheral volumetric bone mineral density in pre- and postmenopausal Chinese women in Hong Kong. Calcif Tissue Int. 2000;67:29–36
  39. Qin L, Au S, Choy W, Leung P, Neff M, Lee K, et al. Regular Tai Chi Chuan exercise may retard bone loss in postmenopausal women: A case-control study. Arch Phys Med Rehabil. 2002;83:1355–1359
  40. Qin L, Au SK, Leung PC, Lau MC, Woo J, Choy WY, et al. Baseline BMD and bone loss at distal radius measured by peripheral quantitative computed tomography in peri- and postmenopausal Hong Kong Chinese women. Osteoporos Int. 2002;13:962–970
  41. Qin L, Choy W, Leung K, Leung PC, Au S, Hung W, et al. Beneficial effects of regular Tai Chi exercise on musculoskeletal system. J Bone Miner Metab. 2005;23:186–190
  42. Recker RR. Bone histomorphometry: techniques and interpretation. Boca Raton, FL: CRC Press; 1983;
  43. Riis BJ, Hansen MA, Jensen AM, Overgaard K, Christiansen C. Low bone mass and fast rate of bone loss at menopause: equal risk factors for future fracture: A 15-year follow-up study. Bone. 1996;19:9–12
  44. Rompe JD, Zoellner J, Nafe B. Shock wave therapy versus conventional surgery in the treatment of calcifying tendinitis of the shoulder. Clin Orthop Relat Res. 2001;387:72–82
  45. Rubin C, Turner AS, Bain S, Mallinckrodt C, McLeodAnabolism K. Low mechanical signals strengthen long bones. Nature. 2001;412:603–604
  46. Rubin C, Turner AS, Mallinckrodt C, Jerome C, McLeod K, Bain S. Mechanical strain, induced noninvasively in the high-frequency domain, is anabolic to cancellous bone, but not cortical bone. Bone. 2002;30:445–452
  47. Rupprecht M, Pogoda P, Mumme M, Rueger JM, Puschel K, Amling M. Bone microarchitecture of the calcaneus and its changes in aging: A histomorphometric analysis of 60 human specimens. J Orthop Res. 2006;24:664–674
  48. Siu WS, Qin L, Cheung WH, Leung KS. A study of trabecular bones in ovariectomized goats with micro-computed tomography and peripheral quantitative computed tomography. Bone. 2004;35:21–26
  49. Suhr D, Brummer F, Irmmer U, Hulser DF. Disturbance of cellular calcium homeostasis by in vitro application of shock waves. Ultrasound Med Biol. 1996;22:671–679
  50. Takahashi K, Yamazaki M, Saisu T, Nakajima A, Shimizu S, Mitsuhashi S, et al. Gene expression for extracellular matrix proteins in shockwave-induced osteogenesis in rats. Calcif Tissue Int. 2004;74:187–193
  51. Tam KF, Cheung WH, Lee KM, Qin L, Leung KS. Delayed stimulatory effect of low-intensity shockwaves on human periosteal cells. Clin Orthop Relat Res. 2005;438:260–265
  52. Tam KF, Cheung WH, Lee KM, Qin L, Leung KS. Osteogenic effects of low-intensity pulsed ultrasound, extracorporeal shockwaves and their combination – an in-vitro comparative study on human periosteal cells. Ultrasound Med Biol. 2008;34:1957–1965
  53. Tischer T, Milz S, Anetzberger H, Muller PE, Wirtz DC, Schmitz C, et al. Extracorporeal shock waves induce ventral-periosteal new bone formation out of the focus zone—results of an in-vivo animal trial. [Article in German] Z Orthop Ihre Grenzgeb. 2002;140:281–285
  54. Tischer T, Milz S, Weiler C, Pautke C, Hausdorf J, Schmitz C. Dose-dependent new bone formation by extracorporeal shock wave application on the intact femur of rabbits. Eur Surg Res. 2008;41:44–53
  55. Turner AS, Alvis M, Myers W, Stevens ML, Lundy MW. Changes in bone mineral density and bone-specific alkaline phosphatase in ovariectomized ewes. Bone. 1995;17:S395–S402
  56. Turner AS, Mallinckrodt CH, Alvis MR, Bryant HU. Dose-response effects of estradiol implants on bone mineral density in ovariectomized ewes. Bone. 1995;17:S421S–427
  57. Wang CJ, Chen HS, Chen CE, Yang KD. Treatment of nonunions of long bone fractures with shock waves. Clin Orthop Relat Res. 2001;387:95–101
  58. Wang FS, Wang CJ, Sheen-Chen SM, Kuo YR, Chen RF, Yang KD. Superoxide mediates shock wave induction of ERK-dependent osteogenic transcription factor (CBFA1) and mesenchymal cell differentiation toward osteoprogenitors. J Biol Chem. 2002;277:10931–10937
  59. Wang FS, Wang CJ, Chen YJ, Chang PR, Huang YT, Sun YC, et al. Ras induction of superoxide activates ERK-dependent angiogenic transcription factor HIF-1alpha and VEGF-A expression in shock wave-stimulated osteoblasts. J Biol Chem. 2004;279:10331–10337
  60. Wang L, Qin L, Lu HB, Cheung WH, Yang H, Wong WN, et al. Extracorporeal shock wave therapy in treatment of delayed bone-tendon healing. Am J Sports Med. 2008;36:340–347
  61. Warden SJ, Bennell KL, Matthews B, Brown DJ, McMeeken JM, Wark JD. Efficacy of low-intensity pulsed ultrasound in the prevention of osteoporosis following spinal cord injury. Bone. 2001;29:431–436
  62. Wolff I, van Croonenborg JJ, Kemper HC, Kostense PJ, Twisk JW. The effect of exercise training programs on bone mass: A meta-analysis of published controlled trials in pre- and postmenopausal women. Osteoporos Int. 1999;9:1–12
  63. Zhang G, Qin L, Shi Y. Epimedium-derived phytoestrogen flavonoids exert beneficial effect on preventing bone loss in late postmenopausal women: A 24-month randomized, double-blind and placebo-controlled trial. J Bone Miner Res. 2007;22:1072–1079

PII: S0301-5629(09)00003-9

doi: 10.1016/j.ultrasmedbio.2009.01.001

Ultrasound in Medicine and Biology
Volume 35, Issue 7 , Pages 1109-1118 , July 2009