The potential benefits and inherent risks of vibration as a non-drug therapy for the prevention and treatment of osteoporosis

Current Osteoporosis Reports

Volumn 11, Issue 1, 2013, Pages 36-44

  Chan, M Ete ^a   Uzer, Gunes ^a   Rubin, Clinton T ^a  

^a St Francis Hospital The Heart Center   (United States)

Author keywords

Biomechanics; Fluid shear; Hematopoietic stem cells; Low intensity vibration; Mechanosensitivity; Mesenchymal stem cells; Nucleus motion; Osteopenia; Sarcopenia

Indexed keywords

PLACEBO;

ARTICLE; BIOMECHANICS; BONE METABOLISM; BONE REMODELING; BONE STRESS; CELL DIFFERENTIATION; CELL FATE; EVIDENCE BASED MEDICINE; HEMATOPOIETIC STEM CELL; HUMAN; LOW INTENSITY VIBRATION; MECHANOTRANSDUCTION; MESENCHYMAL STEM CELL; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; OSTEOPOROSIS; PATIENT SAFETY; PATIENT SATISFACTION; PHYSICAL MEDICINE; POSTMENOPAUSE OSTEOPOROSIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK BENEFIT ANALYSIS; THERAPY EFFECT; WHOLE BODY VIBRATION;

ANIMALS; BONE AND BONES; BONE REMODELING; DISEASE MODELS, ANIMAL; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICE; OSTEOPOROSIS; RISK ASSESSMENT; VIBRATION;

EID: 84882916080     PISSN: 15441873     EISSN: 15442241     Source Type: Journal    
DOI: 10.1007/s11914-012-0132-1     Document Type: Article

References (78)

1. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis, in WHO technical report series 1994, World Health Organization.
2. Bilezikian JP, Matsumoto T, Bellido T, et al. Targeting bone remodeling for the treatment of osteoporosis: summary of the proceedings of an ASBMR workshop. J Bone Miner Res. 2009;24(3):373-85.
3. Iwasaki T, Nonoda Y, Ishii M. Long-term outcomes of children and adolescents who had cerebral palsy with secondary osteoporosis. Curr Med Res Opin. 2012;28(5):737-47.
4. Smith SM, Wastney ME, O'Brien KO, et al. Bone markers, calcium metabolism, and calcium kinetics during extended-duration space flight on the Mir space station. J Bone Miner Res. 2005;20(2):208-18.
5. Leblanc AD, Schneider VS, Evans HJ, et al. Bone mineral loss and recovery after 17 weeks of bed rest. J Bone Miner Res. 1990;5(8):843-50.
6. Vico L, Collet P, Guignandon A, et al. Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts. Lancet. 2000;355(9215):1607-11.
7. Compston JE. Skeletal actions of intermittent parathyroid hormone: effects on bone remodeling and structure. Bone. 2007;40(6):1447-52.
8. Ominsky MS, Vlasseros F, Jolette J, et al. Two doses of sclerostin antibody in cynomolgus monkeys increases bone formation, bone mineral density, and bone strength. J Bone Miner Res. 2010;25(5):948-59.
9. Boonen S, Kay R, Cooper C, et al. Osteoporosis management: a perspective based on bisphosphonate data from randomized clinical trials and observational databases. Int J Clin Pract. 2009;63(12):1792-804.
10. Ohta H. Effects of SERMs on bone health. Evidence for the selective estrogen receptor modulator raloxifene: its evolving role in the treatment of osteoporosis. Clin Calcium. 2010;20(3):315-21.
11. Rubin CT, Lanyon LE. Limb mechanics as a function of speed and gait: a study of functional strains in the radius and tibia of horse and dog. J Exp Biol. 1982;101:187-211.
12. Rubin CT, Lanyon LE. Dynamic strain similarity in vertebrates; an alternative to allometric limb bone scaling. J Theor Biol. 1984;107(2):321-7.
13. Fritton SP, McLeod KJ, Rubin CT. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. J Biomech. 2000;33(3):317-25.
14. Lanyon LE, Rubin CT. Static vs dynamic loads as an influence on bone remodeling. J Biomech. 1984;17(12):897-905.
15. Pel JJ, Bagheri J, van Dam LM, et al. Platform accelerations of three different whole-body vibration devices and the transmission of vertical vibrations to the lower limbs. Med Eng Phys. 2009;31(8):937-44.
16. Issurin VB, Tenenbaum G. Acute and residual effects of vibratory stimulation on explosive strength in elite and amateur athletes. J Sports Sci. 1999;17(3):177-82.
17. Issurin VB, Liebermann DG, Tenenbaum G. Effect of vibratory stimulation training on maximal force and flexibility. J Sports Sci. 1994;12(6):561-6.
18. Bosco C, Iacovelli M, Tsarpela O, et al. Hormonal responses to whole-body vibration in men. Eur J Appl Physiol. 2000;81(6):449-54.
19. Gerodimos V, Zafeiridis A, Karatrantou K, et al. The acute effects of different whole-body vibration amplitudes and frequencies on flexibility and vertical jumping performance. J Sci Med Sport. 2010;13(4):438-43.
20. Wang H, Wan Y, Tam KF, et al. Resistive vibration exercise retards bone loss in weight-bearing skeletons during 60 days bed rest. Osteoporos Int. 2012;23(8):2169-78.
21. Gilsanz V, Wren TAL, Sanchez M, et al. Low-level, high-frequency mechanical signals enhance musculoskeletal development of young women with low BMD. J Bone Miner Res. 2006;21(9):1464-74.
22. Ward K, Alsop C, Caulton J, et al. Low magnitude mechanical loading is osteogenic in children with disabling conditions. J Bone Miner Res. 2004;19(3):360-9.
23. Wren TAL, Lee DC, Hara R, et al. Effect of high-frequency, low-magnitude vibration on bone and muscle in children with cerebral palsy. J Pediatr Orthop. 2010;30(7):732-8.
24. Verschueren SMP, Roelants M, Delecluse C, et al. Effect of 6-month whole body vibration training on hip density, muscle strength, and postural control in postmenopausal women: a randomized controlled pilot study. J Bone Miner Res. 2004;19(3):352-9.
25. Gusi N, Raimundo A, Leal A. Low-frequency vibratory exercise reduces the risk of bone fracture more than walking: a randomized controlled trial. BMC Musculoskelet Disord. 2006;7:92.
26. Iwamoto J, Takeda T, Sato Y, Uzawa M. Effect of whole-body vibration exercise on lumbar bone mineral density, bone turnover, and chronic back pain in post-menopausal osteoporotic women treated with alendronate. Aging Clin Exp Res. 2005;17(2):157-63.
27. Leonard M, Shults J, Zemel B, et al. Effects of low magnitude mechanical signals (LMMS) on bone density and structure in pediatric Crohn's disease: a randomized trial. Minneapolis: The American Society for Bone and Mineral Research; 2012.
28. Rubin C, Recker R, Cullen D, et al. Prevention of postmenopausal bone loss by a low-magnitude, high-frequency mechanical stimuli: a clinical trial assessing compliance, efficacy, and safety. J Bone Miner Res. 2004;19(3):343-51.
29. Drerup B, Granitzka M, Assheuer J, Zerlett G. Assessment of disc injury in subjects exposed to long-term whole-body vibration. Eur Spine J. 1999;8(6):458-67.
30. Griffin JJ. Handbook of Human Vibration. London: Academic Press; 2001.
31. Cummings SR, Black DM, Nevitt MC, et al. Bone density at various sites for prediction of hip fractures. The Study of Osteoporotic Fractures Research Group Lancet. 1993;341(8837):72-5.
32. Judex S, Lei X, Han D, Rubin C. Low-magnitude mechanical signals that stimulate bone formation in the ovariectomized rat are dependent on the applied frequency but not on the strain magnitude. J Biomech. 2007;40(6):1333-9.
33. Hannan MT, Cheng DM, Green E, et al. Establishing the compliance in elderly women for use of a low level mechanical stress device in a clinical osteoporosis study. Osteoporos Int. 2004;15(11):918-26.
34. Rubin C, Gross T, Qin YX, et al. Differentiation of the bone-tissue remodeling response to axial and torsional loading in the turkey ulna. J Bone Joint Surg Am. 1996;78(10):1523-33.
35. Sun YQ, McLeod KJ, Rubin CT. Mechanically induced periosteal bone formation is paralleled by the upregulation of collagen type one mRNA in osteocytes as measured by in situ reverse transcript-polymerase chain reaction. Calcif Tissue Int. 1995;57(6):456-62.
36. Rubin C, Turner AS, Bain S, et al. Anabolism: low mechanical signals strengthen long bones. Nature. 2001;412(6847):603-4.
37. Rubin C, Turner AS, Mallinckrodt C, et al. Mechanical strain, induced noninvasively in the high-frequency domain, is anabolic to cancellous bone, but not cortical bone. Bone. 2002;30(3):445-52.
38. Rubin C, Turner AS, Muller R, et al. Quantity and quality of trabecular bone in the femur are enhanced by a strongly anabolic, noninvasive mechanical intervention. J Bone Miner Res. 2002;17(2):349-57.
39. Oxlund BS, Ortoft G, Andreassen TT, Oxlund H. Low-intensity, high-frequency vibration appears to prevent the decrease in strength of the femur and tibia associated with ovariectomy of adult rats. Bone. 2003;32(1):69-77.
40. Shi HF, Cheung WH, Qin L, et al. Low-magnitude high-frequency vibration treatment augments fracture healing in ovariectomy-induced osteoporotic bone. Bone. 2010;46(5):1299-305.
41. Judex S, Donahue LR, Rubin C. Genetic predisposition to low bone mass is paralleled by an enhanced sensitivity to signals anabolic to the skeleton. FASEB J. 2002;16(10):1280-2.
42. Xie L, Jacobson JM, Choi ES, et al. Low-level mechanical vibrations can influence bone resorption and bone formation in the growing skeleton. Bone. 2006;39(5):1059-66.
43. Ozcivici E, Garman R, Judex S. High-frequency oscillatory motions enhance the simulated mechanical properties of non-weight bearing trabecular bone. J Biomech. 2007;40(15):3404-11.
44. Garman R, Gaudette G, Donahue LR, et al. Low-level accelerations applied in the absence of weight bearing can enhance trabecular bone formation. J Orth Res. 2007;25(6):732-40.
45. Judex S, Garman R, Squire M, et al. Genetically linked site-specificity of disuse osteoporosis. J Bone Miner Res. 2004;19(4):607-13.
46. Rubin C, Xu G, Judex S. The anabolic activity of bone tissue, suppressed by disuse, is normalized by brief exposure to extremely low-magnitude mechanical stimuli. FASEB J. 2001;15(12):2225-9.
47. • Chan ME, Adler BJ, Green DE, Rubin CT. Bone structure and B-cell populations, crippled by obesity, are partially rescued by brief daily exposure to low-magnitude mechanical signals. FASEB J. 2012;26(12):4855-63. While bone remodeling involves the coupling of bone formation and bone resorption activities, most previous studies focused on only the influence of LIV on the bone formation side. This study, however, explored the effect of LIV on the bone resorption aspect by evaluating not only the activity of bone-resorbing osteoclasts but also the differentiation fate of their progenitor HSCs, demonstrating that LIV restores both bone structure and immune B- and T-cells in obese animals through biasing the dichotomous early differentiation pathway of HSCs away from osteoclastogenesis and towards lymphopoiesis.
48. • Luu YK, Capilla E, Rosen CJ, et al. Mechanical stimulation of mesenchymal stem cell proliferation and differentiation promotes osteogenesis while preventing dietary-induced obesity. J Bone Miner Res. 2009;24(1):50-61. Looking beyond the effects of LIV on the terminally differentiated bone-forming osteoblasts that are directly involved in bone formation, this study shows that LIV promotes bone formation and prevents obesity by biasing the fate of their progenitor MSCs towards osteoblastogenesis and away from adipogenesis.
49. Judex S, Boyd S, Qin YX, et al. Adaptations of trabecular bone to low magnitude vibrations result in more uniform stress and strain under load. Ann Biomed Eng. 2003;31(1):12-20.
50. Jee WS, Yao W. Overview: animal models of osteopenia and osteoporosis. J Musculoskelet Neuronal Interact. 2001;1(3):193-207.
51. Goodship AE, Lawes TJ, Rubin CT. Low-magnitude high-frequency mechanical signals accelerate and augment endochondral bone repair: preliminary evidence of efficacy. J Orth Res. 2009;27(7):922-30.
52. Ehrlich PJ, Lanyon LE. Mechanical strain and bone cell function: a review. Osteoporos Int. 2002;13(9):688-700.
53. • Ozcivici E, Luu YK, Rubin CT, Judex S. Low-level vibrations retain bone marrow's osteogenic potential and augment recovery of trabecular bone during reambulation. PLoS One. 2010;5(6):e11178. Corroborating the positive result of LIV on the osteoblastogenesis of MSCs, this study further demonstrates that LIV preserves the osteogenic potential of bone marrow progenitor cells even during bone disuse, and that upon re-ambulation, the recovery of bone morphology is enhanced.
54. Judex S, Zhong N, Squire ME, et al. Mechanical modulation of molecular signals, which regulate anabolic and catabolic activity in bone tissue. J Cell Biochem. 2005;94(5):982-94.
55. O'Rourke RW, Kay T, Scholz MH, et al. Alterations in T-cell subset frequency in peripheral blood in obesity. Obes Surg. 2005;15(10):1463-8.
56. Sato Mito N, Suzui M, Yoshino H, et al. Long term effects of high fat and sucrose diets on obesity and lymphocyte proliferation in mice. J Nutr Health Aging. 2009;13(7):602-6.
57. Patel MJ, Chang KH, Sykes MC, et al. Low magnitude and high frequency mechanical loading prevents decreased bone formation responses of 2T3 preosteoblasts. J Cell Biochem. 2009;106(2):306-16.
58. Dickerson DA, Sander EA, Nauman EA. Modeling the mechanical consequences of vibratory loading in the vertebral body: microscale effects. Biomech Model Mechanobiol. 2008;7(3):191-202.
59. • Lau E, Al-Dujaili S, Guenther A, et al. Effect of low-magnitude, high-frequency vibration on osteocytes in the regulation of osteoclasts. Bone. 2010;46(6):1508-15. This in vitro study illustrated that LIV could influence bone remodeling activities through regulating the interplay between different bone cell types including osteoclast and osteocyte.
60. Sen B, Xie Z, Case N, et al. Mechanical signal influence on mesenchymal stem cell fate is enhanced by incorporation of refractory periods into the loading regimen. J Biomech. 2011;44(4):593-9.
61. Zhou Y, Guan X, Zhu Z, et al. Osteogenic differentiation of bone marrow-derived mesenchymal stromal cells on bone-derived scaffolds: effect of microvibration and role of ERK1/2 activation. Eur Cell Mater. 2011;22:12-25.
62. Tirkkonen L, Halonen H, Hyttinen J, et al. The effects of vibration loading on adipose stem cell number, viability, and differentiation towards bone-forming cells. J R Soc Interface. 2011;8(65):1736-47.
63. Maniotis AJ, Chen CS, Ingber DE. Demonstration of mechanical connections between integrins cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci USA. 1997;94(3):849-54.
64. Hu SH, Chen JX, Butler JP, Wang N. Prestress mediates force propagation into the nucleus. Biochem Biophys Res Commun. 2005;329(2):423-8.
65. Sen B, Guilluy C, Xie Z, et al. Mechanically induced focal adhesion assembly amplifies anti-adipogenic pathways in mesenchymal stem cells. Stem Cells. 2011;29(11):1829-36.
66. Dumas V, Ducharne B, Perrier A, et al. Extracellular matrix produced by osteoblasts cultured under low-magnitude, high-frequency stimulation is favorable to osteogenic differentiation of mesenchymal stem cells. Calcif Tissue Int. 2010;87(4):351-64.
67. Rosenberg N, Levy M, Francis M. Experimental model for stimulation of cultured human osteoblast-like cells by high frequency vibration. Cytotechnology. 2002;39(3):125-30.
68. • Bacabac RG, Smit TH, Van Loon JJWA, et al. Bone cell responses to high-frequency vibration stress: does the nucleus oscillate within the cytoplasm? FASEB J. 2006;20(7):858-64. Through the study of bone cell responses to a wide frequency range, this study implicates that bone cells may sense and respond to high frequency LIV in a distinct mechanism driven by acceleration-induced nucleus oscillations.
69. Zhang X, Schwarz EM, Young DA, et al. Cyclooxygenase-2 regulates mesenchymal cell differentiation into the osteoblast lineage and is critically involved in bone repair. J Clin Invest. 2002;109(11):1405-15.
70. Holguin N, Uzer G, Chiang FP, et al. Brief daily exposure to low-intensity vibration mitigates the degradation of the intervertebral disc in a frequency-specific manner. J Appl Physiol. 2011;111(6):1846-53.
71. • Uzer G, Manske S, Chan M, et al. Separating fluid shear stress from acceleration during vibrations in vitro: identification of mechanical signals modulating the cellular response. Cell Mol Bioeng. 2012;5(3):266-76. To improve the understanding of the contribution of different mechanical signals induced by LIV, this study shows that during LIV treatment, mechanical information carried to the cells can be effectively separated into 2 components: acceleration and the fluid stress, which is a function of the frequency, acceleration and fluid viscosity. Further, in an in-vitro experiment, the peak shear stress can be effectively separated from the peak acceleration by controlling the frequency, acceleration, and/or fluid viscosity of LIV. Further, combining the information of mechanical signals with in vitro cell experiment, this study suggests that, rather than sensing deformation at the cell membrane from "outside-in", bone cells may respond to LIV from "inside-out" through the acceleration-induced movement of the internal cellular structure.
72. Shafrir Y, Forgacs G. Mechanotransduction through the cytoskeleton. Am J Physiol Cell Physiol. 2002;282(3):C479-86.
73. Coughlin TR, Niebur GL. Fluid shear stress in trabecular bone marrow due to low-magnitude high-frequency vibration. J Biomech. 2012;45(13):2222-9.
74. Arnsdorf EJ, Tummala P, Kwon RY, Jacobs CR. Mechanically induced osteogenic differentiation - the role of RhoA, ROCKII, and cytoskeletal dynamics. J Cell Sci. 2009;122(4):546-53.
75. Klein-Nulend J, Semeins CM, Ajubi NE, et al. Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts - correlation with prostaglandin upregulation. Biochem Biophys Res Commun. 1995;217(2):640-8.
76. Klein-Nulend J, van der Plas A, Semeins CM, et al. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J. 1995;9(5):441-5.
77. Muir J, Judex S, Qin YX, Rubin C. Postural instability caused by extended bed rest is alleviated by brief daily exposure to low magnitude mechanical signals. Gait Posture. 2011;33(3):429-35.
78. Rajapakse C. Micro-MRI based biomechanics indicates strength and stiffness of the tibia are improved by brief daily exposure to low magnitude mechanical signals in patients with end-stage renal disease. Minneapolis: The American Society for Bone and Mineral Research; 2012.