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

Ultrasound in Medicine and Biology

Volumn 35, Issue 7, 2009, Pages 1109-1118

  Tam, Kam Fai ^a   Cheung, Wing Hoi ^a   Lee, Kwong Man ^a   Qin, Ling ^a   Leung, Kwok Sui ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Extracorporeal shockwave; Histomorphology; Microarchitecture; Osteoporosis; Trabecular thickness

Indexed keywords

EXTRACORPOREAL SHOCKWAVE; HISTOMORPHOLOGY; MICROARCHITECTURE; OSTEOPOROSIS; TRABECULAR THICKNESS;

CALCIUM; COMPUTERIZED TOMOGRAPHY; MINERALS; MINING; SILICATE MINERALS; TOMOGRAPHY;

BONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; CALCANEUS; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; EXTRACORPOREAL LITHOTRIPSY; FEMALE; FEMUR CONDYLE; GOAT; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; NONHUMAN; OSSIFICATION; OSTEOPOROSIS; OVARIECTOMY; PRIORITY JOURNAL; RADIUS; TRABECULAR BONE; TREATMENT DURATION; TREATMENT RESPONSE;

ANIMALS; BONE DENSITY; CALCANEUS; DISEASE MODELS, ANIMAL; FEMALE; FEMUR; GOATS; HIGH-ENERGY SHOCK WAVES; OSTEOGENESIS; OSTEOPOROSIS; OVARIECTOMY; RADIUS; X-RAY MICROTOMOGRAPHY;

EID: 67649202241     PISSN: 03015629     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ultrasmedbio.2009.01.001     Document Type: Article

References (63)

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