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Ovariectomy Sensitizes Rat Cortical Bone to Whole-Body Vibration

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Abstract

This study was designed to determine the modulatory effect of estrogen on mechanical stimulation in bone. Trabecular and cortical bone compartments of ovariectomized rats exposed to whole-body vibration of different amplitudes were evaluated by peripheral quantitative computed tomographic (pQCT) analysis and histomorphometry and compared to controls not exposed to vibration. Rats underwent whole-body vibration (20 minutes/day, 5 days/week) on a vibration platform for 2 months. The control rats were placed on the platform without vibration for the same time. We divided rats into six groups: a sham control (SHAM); a sham vibrated (SHAM-V) at 30 Hz, 0.6 g; a SHAM-V at 30 Hz, 3g; an ovariectomized control (OVX); an ovariectomized vibrated (OVX-V) at 30 Hz, 0.6 g; and an OVX-V at 30 Hz, 3g. In vivo, pQCT analyses of the tibiae were performed at the start of the experiment and after 4 and 8 weeks. After 8 weeks the tibiae were excised for histomorphometric and for in vitro pQCT analyses. In the SHAM-V group, vibration had no effect upon the different bone parameters. In the OVX-V group, vibration induced a significant increase compared to the OVX group of the cortical and medullary areas (P < 0.01) and of the periosteal (P < 0.01) and endosteal (P < 0.05) perimeters at the 3 g vibration. The strain strength index increased in the OVX-V group significantly (P < 0.01) at the higher vibration. The results showed that low-amplitude, high-frequency whole-body vibration is anabolic to bone in OVX animals. The osteogenic potential is limited to the modeling of the bone cortex and depends on the amplitude of the vibration.

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References

  1. Rubin CT, Mcleod KJ, Bain SD (1990) Functional strains and cortical bone adaptation: epigenetic assurance of skeletal integrity. J Biomech 23(Suppl 1):43–54

    Article  PubMed  Google Scholar 

  2. Rubin CT, Sommerfield DW, Judex S, Qin Y (2001) Inhibition of osteopenia by low magnitude, high frequency mechanical stimuli. Drug Discov Today 6:848–858

    Article  PubMed  Google Scholar 

  3. Rubin CT, Turner AS, Bain S, Mallinckrodt C, McLeod K (2001) Anabolism. Low mechanical signals strengthen long bones. Nature 412:603–604

    Article  PubMed  CAS  Google Scholar 

  4. Jankovich JP (1972) The effects of mechanical vibration on bone development in the rat. J Biomech 5:241–250

    Article  PubMed  CAS  Google Scholar 

  5. Rubin C, Turner AS, Mallinckrodt C, Jerome C, Mcleod K, Bain S (2002) Mechanical strain, induced noninvasively in the high-frequency domain, is anabolic to cancellous bone, but not cortical bone. Bone 30:445–52

    Article  PubMed  CAS  Google Scholar 

  6. Judex S, Zhong N, Squire ME, Ye K, Donahue LR, Hadjiargyrou M, Rubin CT (2005) Mechanical modulation of molecular signals which regulate anabolic and catabolic activity in bone tissue. J Cell Biochem 94:982–994

    Article  PubMed  Google Scholar 

  7. Tanaka SM, Li J, Duncan RL, Yokota H, Burr DB, Turner CH (2003) Effects of broad frequency vibration on cultured osteoblasts. J Biomech 36:73–80

    Article  PubMed  Google Scholar 

  8. Usui Y, Zerwekh JE, Vanharanta H, Ashman RB, Mooney V (1989) Different effects of mechanical vibration on bone ingrowth into porous hydroxyapatite and fracture healing in a rabbit model. J Orthop Res 7:559–567

    Article  PubMed  CAS  Google Scholar 

  9. Tanaka SM, Alam I, Turner CH (2003) Stochastic resonance in osteogenic response to mechanical loading. FASEB J 17:313–314

    PubMed  CAS  Google Scholar 

  10. Oxlund BS, Ortoft G, Andreassen TT, Oxlund H (2003) Low-intensity, high-frequency vibration appears to prevent the decrease in strength of the femur and tibia associated with ovariectomy of adult rats. Bone 32:69–77

    Article  PubMed  CAS  Google Scholar 

  11. Flieger J, Karachalios TH, Khaldi L, Raptou P, Lyritis G (1998) Mechanical stimulation in the form of vibration prevents postmenopausal bone loss in ovariectomized rats. Calcif Tissue Int 63:510–514

    Article  PubMed  CAS  Google Scholar 

  12. Frost HM (1987) Bone mass and the mechanostat: a proposal. Anat Rec 219:1–9

    Article  PubMed  CAS  Google Scholar 

  13. Frost HM (1983) A determinant of bone architecture. The minimum effective strain. Clin Orthop 175:286–292

    PubMed  Google Scholar 

  14. Frost HM (1987) The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and non mechanical agents. Bone Miner 2:73–85

    PubMed  CAS  Google Scholar 

  15. Lanyon LE, Sherry TM (2001) Perspective. Postmenopausal osteoporosis as a failure of bone’s adaptation to functional loading: a hypothesis. J Bone Miner Res 16:1937–1947

    Article  PubMed  CAS  Google Scholar 

  16. Lanyon LE, Armstrong V, Ong D, Zaman G, Price J (2004) Is estrogen receptor α key to controlling bones’ resistence to fracture? J Endocrinol 182:183–191

    Article  PubMed  CAS  Google Scholar 

  17. Jessop HL, Sjoberg M, Cheng MZ, Zaman G, Weeler-Jones CP, Lanyon LE (2001) Mechanical strain and estrogen activate estrogen receptor alpha in bone cells. J Bone Miner Res 16:1045–1055

    Article  PubMed  CAS  Google Scholar 

  18. Ehrlich PJ, Noble BS, Jessop HL, Stevens HY, Mosley JR, Lanyon LE (2002) The effect of in vivo mechanical loading on estrogen receptor alpha expression in rat ulnar osteocytes. J Bone Miner Res 17:1646–1655

    Article  PubMed  CAS  Google Scholar 

  19. Lee K, Jessop HL, Suswillo R, Zaman G, Lanyon L (2003) Endocrinology: bone adaptation requires oestrogen receptor-alpha. Nature 424:389

    Article  PubMed  CAS  Google Scholar 

  20. Zaman G, Jessop HL, Muzylak M, De Souza RL, Pitsillides AA, Price JS, Lanyon LL (2006) Osteocytes use estrogen receptor α to respond to strain but their ERα content is regulated by estrogen. J Bone Miner Res 21:1297–1306

    Article  PubMed  Google Scholar 

  21. Bass SL, Saxon LK, Daly RM, Turner CH, Robling AG, Seeman E, Stuckey S (2002) The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res 17:2274–2280

    Article  PubMed  CAS  Google Scholar 

  22. Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK (2003) Bone loss and bone size after menopause. N Engl J Med 349:327–334

    Article  PubMed  Google Scholar 

  23. Vanderschueren D, Venken K, Ophoff J, Bouillon R, Boonen S (2006) Sex steroids and the periosteum: reconsidering the roles of androgens and estrogens in periosteal expansion. J Clin Endocrinol Metab 91:378–382

    Article  PubMed  Google Scholar 

  24. Duan Y, Beck TJ, Wang XF, Seeman E (2003) Structural and biomechanical basis of sexual dimorphism in femoral neck fragility has its origins in growth and aging. J Bone Miner Res 18:1766–1774

    Article  PubMed  Google Scholar 

  25. Bouillon R, Bex M, Vanderschueren D, Boonen S (2004) Estrogens are essential for male pubertal periosteal bone expansion. J Clin Endocrinol Metab 89:6025–6029

    Article  PubMed  CAS  Google Scholar 

  26. Saxon LK, Turner CH (2005) Estrogen receptor β: the antimechanostat? Bone 36:185–192

    Article  PubMed  CAS  Google Scholar 

  27. Westerlind KC, Wronski TJ, Ritman EL, Luo ZP, An KN, Bell NH, Turner RT (1997) Estrogen regulates the rate of bone turnover but bone balance in ovariectomized rats is modulated by prevailing mechanical strain. Proc Natl Acad Sci USA 94:4199–4204

    Article  PubMed  CAS  Google Scholar 

  28. Gilsanz V, Wren TA, Sanchez M, Dorey F, Judex S, Rubin C (2006) Low-level, high-frequency mechanical signals enhance musculoskeletal development of young women with low BMD. J Bone Miner Res 21:1464–1474

    Article  PubMed  Google Scholar 

  29. Torvinen S, Kannus P, Sievanen H, Jarvinen TA, Pasanen M, Kontulainen S, Nenonen A, Jarvinen TL, Paakkala T, Jarvinen M, Vuori I (2003) Effect of 8-month vertical whole-body vibration on bone, muscle performance, and body balance: a randomized controlled study. J Bone Miner Res 18: 876–884

    Article  PubMed  Google Scholar 

  30. Rabkin BA, Szivek JA, Schonfeld JE, Halloran BP (2001) Long term measurement of bone strain in vivo: the rat tibia. J Biomed Mater Res B Appl Biomater 58:277–281

    Article  CAS  Google Scholar 

  31. Ioannidis GV, Skarantavos G, Raptou P, Khaldi L, Karachalios TH, Lyritis GP (2000) Whole-body vibrations induce periosteal bone formation in ovariectomised rats. J Musculoskelet Neuronal Interact 1:70–71

    Google Scholar 

  32. Castillo AB, Alam I, Tanaka SM, Levenda J, Li J, Warden SJ, Turner CH (2006) Low-amplitude, broad-frequency vibration effects on cortical bone in mice. Bone 39:1087–1096

    Article  PubMed  Google Scholar 

  33. Saxon LK, Turner CH (2006) Low-dose estrogen treatment suppresses periosteal bone formation in response to mechanical loading. Bone 39:1261–1267

    Article  PubMed  Google Scholar 

  34. Saxon LK, Robling AG, Castillo AB, Mohan S, Turner CH (2007) The skeletal responsiveness to mechanical loading is enhanced in mice with a null mutation in estrogen receptor-beta. Am J Physiol Endocrinol Metab 293:E484–E491

    Article  PubMed  CAS  Google Scholar 

  35. Seeman E (2007) The periosteum—a surface for all seasons. Osteoporos Int 18:123–128

    Article  PubMed  CAS  Google Scholar 

  36. Garman R, Gaudette G, Donahue LR, Rubin C, Judex S (2007) Low-level accelerations applied in the absence of weight bearing can enhance trabecular bone formation. J Orthop Res 25:732–740

    Article  PubMed  Google Scholar 

  37. Judex S, Lei X, Han D, Rubin C (2007) 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 40:1333–1339

    Article  PubMed  Google Scholar 

  38. Christiansen BA, Silva MJ (2006) The effect of varying magnitudes of whole-body vibration on several skeletal sites in mice. Ann Biomed Eng 34:1149–1156

    Article  PubMed  Google Scholar 

  39. Warden SJ, Turner CH (2004) Mechanotransduction in the cortical bone is most efficient at loading frequencies of 5–10 Hz. Bone 34:261–270

    Article  PubMed  CAS  Google Scholar 

  40. Beamer WG, Donahue LR, Rosen CJ, Baylink DJ (1996) Genetic variability in adult bone density among inbred strains of mice. Bone 18:397–403

    Article  PubMed  CAS  Google Scholar 

  41. Iida H, Fukuda S (2002) Age-related changes in bone mineral density, cross-sectional area and strength at different skeletal sites in male rats. J Vet Med Sci 64:29–34

    Article  PubMed  Google Scholar 

  42. Allen MR, Hock JM, Burr DB (2004) Periosteum: biology, regulation, and response to osteoporosis therapies. Bone 35:1003–1012

    Article  PubMed  CAS  Google Scholar 

  43. Cardinale M, Rittweger J (2006) Vibration exercise makes your muscles and bones stronger: fact or fiction? J Br Menopause Soc 12:12–18

    Article  PubMed  Google Scholar 

  44. Griffin MJ (2004) Minimum health and safety requirements for workers exposed to hand-transmitted vibration and whole-body vibration in the European Union: a review. Occup Environ Med 61:387–397

    Article  PubMed  CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Bone Metabolic Unit, Scientific Institute San Raffaele, Via Olgettina 60, Milan, 20132, Italy

    Alessandro Rubinacci, Massimo Marenzana, Federica Colasante, Isabella Villa, Gian Luigi Moro & Luigi Paolo Spreafico

  2. Department of Anatomy and Histology, University of Modena and Reggio Emilia, Modena, Italy

    Francesco Cavani, Marzia Ferretti & Gastone Marotti

  3. Stratec Medizintechnik, Pforzheim, Germany

    Johannes Willnecker

  4. Department of Pharmacology, Chemotherapy, and Medical Toxicology, University of Milan, Milan, Italy

    Francesca Guidobono

Authors
  1. Alessandro Rubinacci
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  2. Massimo Marenzana
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  3. Francesco Cavani
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  4. Federica Colasante
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Correspondence to Alessandro Rubinacci.

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Rubinacci, A., Marenzana, M., Cavani, F. et al. Ovariectomy Sensitizes Rat Cortical Bone to Whole-Body Vibration. Calcif Tissue Int 82, 316–326 (2008). https://doi.org/10.1007/s00223-008-9115-8

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  • DOI: https://doi.org/10.1007/s00223-008-9115-8

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