Skip to main content

Advertisement

Log in

Bone architecture adaptations after spinal cord injury: impact of long-term vibration of a constrained lower limb

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

This study examined the effect of a controlled dose of vibration upon bone density and architecture in people with spinal cord injury (who eventually develop severe osteoporosis). Very sensitive computed tomography (CT) imaging revealed no effect of vibration after 12 months, but other doses of vibration may still be useful to test.

Introduction

The purposes of this report were to determine the effect of a controlled dose of vibratory mechanical input upon individual trabecular bone regions in people with chronic spinal cord injury (SCI) and to examine the longitudinal bone architecture changes in both the acute and chronic state of SCI.

Methods

Participants with SCI received unilateral vibration of the constrained lower limb segment while sitting in a wheelchair (0.6g, 30 Hz, 20 min, three times weekly). The opposite limb served as a control. Bone mineral density (BMD) and trabecular micro-architecture were measured with high-resolution multi-detector CT. For comparison, one participant was studied from the acute (0.14 year) to the chronic state (2.7 years).

Results

Twelve months of vibration training did not yield adaptations of BMD or trabecular micro-architecture for the distal tibia or the distal femur. BMD and trabecular network length continued to decline at several distal femur sub-regions, contrary to previous reports suggesting a “steady state” of bone in chronic SCI. In the participant followed from acute to chronic SCI, BMD and architecture decline varied systematically across different anatomical segments of the tibia and femur.

Conclusions

This study supports that vibration training, using this study’s dose parameters, is not an effective anti-osteoporosis intervention for people with chronic SCI. Using a high-spatial-resolution CT methodology and segmental analysis, we illustrate novel longitudinal changes in bone that occur after spinal cord injury.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Qin W, Bauman WA, Cardozo CP (2010) Evolving concepts in neurogenic osteoporosis. Curr Osteoporos Rep 8:212–218

    Article  PubMed  Google Scholar 

  2. Edwards WB, Schnitzer TJ, Troy KL (2014) Bone mineral and stiffness loss at the distal femur and proximal tibia in acute spinal cord injury. Osteoporos Int 25:1005–1015

    Article  CAS  PubMed  Google Scholar 

  3. Dudley-Javoroski S, Shields RK (2012) Regional cortical and trabecular bone loss after spinal cord injury. J Rehabil Res Dev 49:1365–1376

    Article  PubMed  PubMed Central  Google Scholar 

  4. Dudley-Javoroski S, Saha PK, Liang G, Li C, Gao Z, Shields RK (2012) High dose compressive loads attenuate bone mineral loss in humans with spinal cord injury. Osteoporos Int 23:2335–2346

    Article  CAS  PubMed  Google Scholar 

  5. Dudley-Javoroski S, Shields RK (2008) Asymmetric bone adaptations to soleus mechanical loading after spinal cord injury. J Musculoskelet Neuronal Interact 8:227–238

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Dudley-Javoroski S, Shields RK (2013) Active-resisted stance modulates regional bone mineral density in humans with spinal cord injury. J Spinal Cord Med 36:191–199

    Article  PubMed  PubMed Central  Google Scholar 

  7. Shields RK, Dudley-Javoroski S (2006) Musculoskeletal plasticity after acute spinal cord injury: Effects of long-term neuromuscular electrical stimulation training. J Neurophysiol 95:2380–2390

    Article  PubMed  PubMed Central  Google Scholar 

  8. Hartkopp A, Murphy RJ, Mohr T, Kjaer M, Biering-Sorensen F (1998) Bone fracture during electrical stimulation of the quadriceps in a spinal cord injured subject. Arch Phys Med Rehabil 79:1133–1136

    Article  CAS  PubMed  Google Scholar 

  9. Kern H, Carraro U, Adami N et al (2010) Home-based functional electrical stimulation rescues permanently denervated muscles in paraplegic patients with complete lower motor neuron lesion. Neurorehabil Neural Repair 24:709–721

    Article  PubMed  Google Scholar 

  10. Fritton SP, McLeod KJ, Rubin CT (2000) Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. J Biomech 33:317–325

    Article  CAS  PubMed  Google Scholar 

  11. Garman R, Rubin C, Judex S (2007) Small oscillatory accelerations, independent of matrix deformations, increase osteoblast activity and enhance bone morphology. PLoS ONE 2:e653

    Article  PubMed  PubMed Central  Google Scholar 

  12. Bramlett HM, Dietrich WD, Marcillo A et al (2014) Effects of low intensity vibration on bone and muscle in rats with spinal cord injury. Osteoporos Int

  13. Ozcivici E, Garman R, Judex S (2007) High-frequency oscillatory motions enhance the simulated mechanical properties of non-weight bearing trabecular bone. J Biomech 40:3404–3411

    Article  PubMed  Google Scholar 

  14. 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 30:445–452

    Article  CAS  PubMed  Google Scholar 

  15. Huang RP, Rubin CT, McLeod KJ (1999) Changes in postural muscle dynamics as a function of age. J Gerontol A Biol Sci Med Sci 54:B352–B357

    Article  CAS  PubMed  Google Scholar 

  16. Asselin P, Spungen AM, Muir JW, Rubin CT, Bauman WA (2011) Transmission of low-intensity vibration through the axial skeleton of persons with spinal cord injury as a potential intervention for preservation of bone quantity and quality. J Spinal Cord Med 34:52–59

    Article  PubMed  PubMed Central  Google Scholar 

  17. Davis R, Sanborn C, Nichols D, Bazett-Jones DM, Dugan EL (2010) The effects of whole body vibration on bone mineral density for a person with a spinal cord injury: a case study. Adapt Phys Act Q 27:60–72

    Article  Google Scholar 

  18. Wuermser LA, Beck LA, Lamb JL, Atkinson EJ, Amin S (2014) The effect of low-magnitude whole body vibration on bone density and microstructure in men and women with chronic motor complete paraplegia. J Spinal Cord Med

  19. McHenry CL, Wu J, Shields RK (2014) Potential regenerative rehabilitation technology: implications of mechanical stimuli to tissue health. BMC Res Notes 7:334

    Article  PubMed  PubMed Central  Google Scholar 

  20. Bala Y, Depalle B, Farlay D, Douillard T, Meille S, Follet H, Chapurlat R, Chevalier J, Boivin G (2012) Bone micromechanical properties are compromised during long-term alendronate therapy independently of mineralization. J Bone Miner Res 27:825–834

    Article  CAS  PubMed  Google Scholar 

  21. Rubin CD (2005) Emerging concepts in osteoporosis and bone strength. Curr Med Res Opin 21:1049–1056

    Article  PubMed  Google Scholar 

  22. Giangregorio L, Lala D, Hummel K, Gordon C, Craven BC (2013) Measuring apparent trabecular density and bone structure using peripheral quantitative computed tomography at the tibia: precision in participants with and without spinal cord injury. J Clin Densitom 16:139–146

    Article  PubMed  Google Scholar 

  23. Edwards WB, Schnitzer TJ, Troy KL (2014) The mechanical consequence of actual bone loss and simulated bone recovery in acute spinal cord injury. Bone 60:141–147

    Article  PubMed  Google Scholar 

  24. Edwards WB, Schnitzer TJ, Troy KL (2014) Reduction in proximal femoral strength in patients with acute spinal cord injury. J Bone Miner Res

  25. Kirshblum SC, Burns SP, Biering-Sorensen F, Donovan W, Graves DE, Jha A, Johansen M, Jones L, Krassioukov A, Mulcahey M, Schmidt-Read M, Waring W (2011) International Standards for Neurological Classification of Spinal Cord Injury (Revised 2011). J Spinal Cord Med 34:535–546

    Article  PubMed  PubMed Central  Google Scholar 

  26. Dudley-Javoroski S, Shields RK (2009) Longitudinal changes in femur bone mineral density after spinal cord injury: effects of slice placement and peel method. Osteoporos Int 21:985–995

    Article  PubMed  PubMed Central  Google Scholar 

  27. Saha PK, Xu Y, Duan H, Heiner A, Liang G (2010) Volumetric topological analysis: a novel approach for trabecular bone classification on the continuum between plates and rods. IEEE Trans Med Imaging 29:1821–1838

    Article  PubMed  PubMed Central  Google Scholar 

  28. Wehrli FW, Ladinsky GA, Jones C et al (2008) In vivo magnetic resonance detects rapid remodeling changes in the topology of the trabecular bone network after menopause and the protective effect of estradiol. J Bone Miner Res 23:730–740

    Article  PubMed  PubMed Central  Google Scholar 

  29. 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 

  30. Chang SH, Dudley-Javoroski S, Shields RK (2011) Gravitational force modulates muscle activity during mechanical oscillation of the tibia in humans. J Electromyogr Kinesiol

  31. Chang SH, Tseng SC, McHenry CL, Littmann AE, Suneja M, Shields RK (2012) Limb segment vibration modulates spinal reflex excitability and muscle mRNA expression after spinal cord injury. Clin Neurophysiol 123:558–568

    Article  CAS  PubMed  Google Scholar 

  32. Eser P, Schiessl H, Willnecker J (2004) Bone loss and steady state after spinal cord injury: a cross-sectional study using pQCT. J Musculoskelet Neuronal Interact 4:197–198

    CAS  PubMed  Google Scholar 

  33. Frotzler A, Berger M, Knecht H, Eser P (2008) Bone steady-state is established at reduced bone strength after spinal cord injury: A longitudinal study using peripheral quantitative computed tomography (pQCT). Bone 43:549–555

    Article  PubMed  Google Scholar 

  34. Bauman WA, Spungen AM, Wang J, Pierson RN Jr, Schwartz E (1999) Continuous loss of bone during chronic immobilization: a monozygotic twin study. Osteoporos Int 10:123–127

    Article  CAS  PubMed  Google Scholar 

  35. Shields RK, Dudley-Javoroski S (2007) Musculoskeletal adaptation in chronic spinal cord injury: effects of long-term soleus electrical stimulation training. J Neurorehabil Neural Repair 21:169–179

    Article  Google Scholar 

  36. Frey Law L, Shields RK (2004) Femoral loads during passive, active, and active-resistive stance after spinal cord injury: a mathematical model. Clin Biomech 19:313–321

    Article  Google Scholar 

  37. McHenry CL, Shields RK (2012) A biomechanical analysis of exercise in standing, supine, and seated positions: implications for individuals with spinal cord injury. J Spinal Cord Med 35:140–147

    Article  PubMed  PubMed Central  Google Scholar 

  38. Chilibeck PD, Bell G, Jeon J, Weiss CB, Murdoch G, MacLean I, Ryan E, Burnham R (1999) Functional electrical stimulation exercise increases GLUT-1 and GLUT-4 in paralyzed skeletal muscle. Metabolism 48:1409–1413

    Article  CAS  PubMed  Google Scholar 

  39. Gorgey AS, Mather KJ, Cupp HR, Gater DR (2012) Effects of resistance training on adiposity and metabolism after spinal cord injury. Med Sci Sports Exerc 44:165–174

    Article  CAS  PubMed  Google Scholar 

  40. Griffin L, Decker MJ, Hwang JY, Wang B, Kitchen K, Ding Z, Ivy JL (2008) Functional electrical stimulation cycling improves body composition, metabolic and neural factors in persons with spinal cord injury. J Electromyogr Kinesiol 19:614–622

    Article  PubMed  Google Scholar 

  41. Jeon JY, Hettinga D, Steadward RD, Wheeler GD, Bell G, Harber V (2010) Reduced plasma glucose and leptin after 12 weeks of functional electrical stimulation-rowing exercise training in spinal cord injury patients. Arch Phys Med Rehabil 91:1957–1959

    Article  PubMed  Google Scholar 

  42. Mahoney ET, Bickel CS, Elder C, Black C, Slade JM, Apple D Jr, Dudley GA (2005) Changes in skeletal muscle size and glucose tolerance with electrically stimulated resistance training in subjects with chronic spinal cord injury. Arch Phys Med Rehabil 86:1502–1504

    Article  PubMed  Google Scholar 

  43. Rittweger J, Goosey-Tolfrey VL, Cointry G, Ferretti JL (2010) Structural analysis of the human tibia in men with spinal cord injury by tomographic (pQCT) serial scans. Bone 47:511–518

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by awards to RKS from the National Institutes of Health (R01HD062507), and the Craig H. Neilsen Foundation. We thank Ann Lawler for assistance with manuscript preparation.

Conflicts of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. K. Shields.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dudley-Javoroski, S., Petrie, M.A., McHenry, C.L. et al. Bone architecture adaptations after spinal cord injury: impact of long-term vibration of a constrained lower limb. Osteoporos Int 27, 1149–1160 (2016). https://doi.org/10.1007/s00198-015-3326-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-015-3326-4

Keywords

Navigation