Skip to main content

Advertisement

SpringerLink
Log in

Bone fragility after spinal cord injury: reductions in stiffness and bone mineral at the distal femur and proximal tibia as a function of time

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

Abstract

Summary

Computed tomography and finite element modeling were used to assess bone structure at the knee as a function of time after spinal cord injury. Analyzed regions experienced degradation in stiffness, mineral density, and content. Changes were well described as an exponential decay over time, reaching a steady state 3.5 years after injury.

Introduction

Spinal cord injury (SCI) is associated with bone fragility and an increased risk of fracture around the knee. The purpose of this study was to investigate bone stiffness and mineral content at the distal femur and proximal tibia, using finite element (FE) and computed tomography (CT) measures. A cross-sectional design was used to compare differences between non-ambulatory individuals with SCI as a function of time after injury (0–50 years).

Methods

CT scans of the knee were obtained from 101 individuals who experienced an SCI 30 days to 50 years prior to participation. Subject-specific FE models were used to estimate stiffness under axial compression and torsional loading, and CT data was analyzed to assess volumetric bone mineral density (vBMD) and bone mineral content (BMC) for integral, cortical, and trabecular compartments of the epiphyseal, metaphyseal, and diaphyseal regions of the distal femur and proximal tibia.

Results

Bone degradation was well described as an exponential decay over time (R2 = 0.33–0.83), reaching steady-state levels within 3.6 years of SCI. Individuals at a steady state had 40 to 85% lower FE-derived bone stiffness and robust decreases in CT mineral measures, compared to individuals who were recently injured (t ≤ 47 days). Temporal and spatial patterns of bone loss were similar between the distal femur and proximal tibia.

Conclusions

After SCI, individuals experienced rapid and profound reductions in bone stiffness and bone mineral at the knee. FE models predicted similar reductions to axial and torsional stiffness, suggesting that both failure modes may be clinically relevant. Importantly, CT-derived measures of bone mineral alone underpredicted the impacts of SCI, compared to FE-derived measures of stiffness.

Trial registration

ClinicalTrials.gov (NCT01225055, NCT02325414)

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Jiang S-D, Dai L-Y, Jiang L-S (2006) Osteoporosis after spinal cord injury. Osteoporos Int 17:180–192. https://doi.org/10.1007/s00198-005-2028-8

    Article  PubMed  Google Scholar 

  2. Edwards WB, Schnitzer TJ (2015) Bone imaging and fracture risk after spinal cord injury. Curr Osteoporos Rep 13:310–317. https://doi.org/10.1007/s11914-015-0288-6

    Article  PubMed  Google Scholar 

  3. Edwards WB, Schnitzer TJ, Troy KL (2013) Bone mineral and stiffness loss at the distal femur and proximal tibia in acute spinal cord injury. Osteoporos Int 24:2461–2469. https://doi.org/10.1007/s00198-013-2557-5

    Article  CAS  PubMed  Google Scholar 

  4. Edwards WB, Schnitzer TJ, Troy KL (2014) Reduction in proximal femoral strength in patients with acute spinal cord injury. J Bone Miner Res 29:2074–2079. https://doi.org/10.1002/jbmr.2227

    Article  PubMed  Google Scholar 

  5. Jiang SD, Jiang LS, Dai LY (2006) Mechanisms of osteoporosis in spinal cord injury. Clin Endocrinol 65:555–565. https://doi.org/10.1111/j.1365-2265.2006.02683.x

    Article  CAS  Google Scholar 

  6. Biering-Sorensen F, Bohr HH, Schaadt OP (1990) Longitudinal study of bone mineral content in the lumbar spine, the forearm and the lower extremities after spinal cord injury. Eur J Clin Investig 20:330–335

    Article  CAS  Google Scholar 

  7. Eser P, Frotzler A, Zehnder Y et al (2004) Relationship between the duration of paralysis and bone structure: a pQCT study of spinal cord injured individuals. Bone 34:869–880. https://doi.org/10.1016/j.bone.2004.01.001

    Article  CAS  PubMed  Google Scholar 

  8. Edwards WB, Simonian N, Troy KL, Schnitzer TJ (2015) Reduction in torsional stiffness and strength at the proximal tibia as a function of time since spinal cord injury. J Bone Miner Res 30:1422–1430. https://doi.org/10.1002/jbmr.2474

    Article  CAS  PubMed  Google Scholar 

  9. Vestergaard P, Krogh K, Rejnmark L, Mosekilde L (1998) Fracture rates and risk factors for fractures in patients with spinal cord injury. Spinal Cord 36:790–796. https://doi.org/10.1038/sj.sc.3100648

    Article  CAS  PubMed  Google Scholar 

  10. Keating JF, Kerr M, Delargy M Minimal trauma causing fractures in patients with spinal cord injury. Disabil Rehabil 14:108–109

    Article  CAS  Google Scholar 

  11. Martínez ÁA, Cuenca J, Herrera A, Domingo J (2002) Late lower extremity fractures in patients with paraplegia. Injury 33:583–586. https://doi.org/10.1016/S0020-1383(02)00163-8

    Article  PubMed  Google Scholar 

  12. Morse LR, Battaglino RA, Stolzmann KL et al (2009) Osteoporotic fractures and hospitalization risk in chronic spinal cord injury. Osteoporos Int 20:385–392. https://doi.org/10.1007/s00198-008-0671-6

    Article  CAS  PubMed  Google Scholar 

  13. Gifre L, Vidal J, Carrasco J et al (2014) Incidence of skeletal fractures after traumatic spinal cord injury: a 10-year follow-up study. Clin Rehabil 28:361–369. https://doi.org/10.1177/0269215513501905

    Article  PubMed  Google Scholar 

  14. Carbone LD, Chin AS, Burns SP et al (2014) Mortality after lower extremity fractures in men with spinal cord injury. J Bone Miner Res 29:432–439. https://doi.org/10.1002/jbmr.2050

    Article  PubMed  Google Scholar 

  15. Gifre L, Humbert L, Muxi A, et al (2018) Analysis of the evolution of cortical and trabecular bone compartments in the proximal femur after spinal cord injury by 3D-DXA. Osteoporos Int 29:201–209. https://doi.org/10.1007/s00198-017-4268-9

    Article  Google Scholar 

  16. Garland DE, Stewart CA, Adkins RH et al (1992) Osteoporosis after spinal cord injury. J Orthop Res 10:371–378. https://doi.org/10.1002/jor.1100100309

    Article  CAS  PubMed  Google Scholar 

  17. Cody DD, Gross GJ, Hou FJ et al (1999) Femoral strength is better predicted by finite element models than QCT and DXA. J Biomech 32:1013–1020. https://doi.org/10.1016/S0021-9290(99)00099-8

    Article  CAS  PubMed  Google Scholar 

  18. Edwards WB, Schnitzer TJ, Troy KL (2013) Torsional stiffness and strength of the proximal tibia are better predicted by finite element models than DXA or QCT. J Biomech 46:1655–1662. https://doi.org/10.1016/j.jbiomech.2013.04.016

    Article  PubMed  PubMed Central  Google Scholar 

  19. Falcinelli C, Schileo E, Balistreri L et al (2014) Multiple loading conditions analysis can improve the association between finite element bone strength estimates and proximal femur fractures: a preliminary study in elderly women. Bone 67:71–80. https://doi.org/10.1016/j.bone.2014.06.038

    Article  PubMed  Google Scholar 

  20. Keyak JH, Sigurdsson S, Karlsdottir G et al (2011) Male-female differences in the association between incident hip fracture and proximal femoral strength: a finite element analysis study. Bone 48:1239–1245. https://doi.org/10.1016/j.bone.2011.03.682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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. https://doi.org/10.1016/j.bone.2013.12.012

    Article  PubMed  Google Scholar 

  22. Edwards WB, Schnitzer TJ, Troy KL (2013) Bone mineral loss at the proximal femur in acute spinal cord injury. Osteoporos Int 24:2461–2469. https://doi.org/10.1007/s00198-013-2323-8

    Article  CAS  PubMed  Google Scholar 

  23. Edwards WB, Simonian N, Haider IT et al (2018) Effects of teriparatide and vibration on bone mass and bone strength in people with bone loss and spinal cord injury: a randomized, controlled trial. J Bone Miner Res. https://doi.org/10.1002/jbmr.3525

    Article  CAS  Google Scholar 

  24. Winter DA (2009) Biomechanics and motor control of human movement. John Wiley & Sons, New York

    Book  Google Scholar 

  25. Cheng X, Li J, Lu Y et al (2007) Proximal femoral density and geometry measurements by quantitative computed tomography: association with hip fracture. Bone 40:169–174. https://doi.org/10.1016/j.bone.2006.06.018

    Article  CAS  PubMed  Google Scholar 

  26. Rho JY, Hobatho MC, Ashman RB (1995) Relations of mechanical properties to density and CT numbers in human bone. Med Eng Phys 17:347–355. https://doi.org/10.1016/1350-4533(95)97314-F

    Article  CAS  PubMed  Google Scholar 

  27. Dalstra M, Huiskes R, Odgaard A, van Erning L (1993) Mechanical and textural properties of pelvic trabecular bone. J Biomech 26:523–535. https://doi.org/10.1016/0021-9290(93)90014-6

    Article  CAS  PubMed  Google Scholar 

  28. Rho JY (1996) An ultrasonic method for measuring the elastic properties of human tibial cortical and cancellous bone. Ultrasonics 34:777–783. https://doi.org/10.1016/S0041-624X(96)00078-9

    Article  CAS  PubMed  Google Scholar 

  29. Bauman WA, Spungen AM, Wang J et al (1999) Continuous loss of bone during chronic immobilization: a monozygotic twin study. Osteoporos Int 10:123–127. https://doi.org/10.1007/s001980050206

    Article  CAS  PubMed  Google Scholar 

  30. Allen MP (1997) Understanding regression analysis. Springer, Boston, pp 113–117

    Google Scholar 

  31. Ausk BJ, Huber P, Srinivasan S et al (2013) Metaphyseal and diaphyseal bone loss in the tibia following transient muscle paralysis are spatiotemporally distinct resorption events. Bone 57:413–422. https://doi.org/10.1016/j.bone.2013.09.009

    Article  PubMed  Google Scholar 

  32. Keaveny TM, Kopperdahl DL, Melton LJ et al (2010) Age-dependence of femoral strength in white women and men. J Bone Miner Res 25:994–1001. https://doi.org/10.1002/jbmr.091033

    Article  PubMed  Google Scholar 

  33. De Bruin ED, Vanwanseele B, Dambacher MA et al (2005) Long-term changes in the tibia and radius bone mineral density following spinal cord injury. Spinal Cord 43:96–101. https://doi.org/10.1038/sj.sc.3101685

    Article  PubMed  Google Scholar 

  34. Russo CR, Lauretani F, Seeman E et al (2006) Structural adaptations to bone loss in aging men and women. Bone 38:112–118. https://doi.org/10.1016/j.bone.2005.07.025

    Article  PubMed  Google Scholar 

  35. McCarthy I, Goodship A, Herzog R et al (2000) Investigation of bone changes in microgravity during long and short duration space flight: comparison of techniques. Eur J Clin Investig 30:1044–1054. https://doi.org/10.1046/j.1365-2362.2000.00719.x

    Article  CAS  Google Scholar 

  36. Troy KL, Edwards WB (2018) Practical considerations for obtaining high quality quantitative computed tomography data of the skeletal system. Bone 110:58–65. https://doi.org/10.1016/j.bone.2018.01.013

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank our colleagues Dr. Alan S. Anschel, Dr. David Chen, and Dr. Ki H. Kim at the Shirley Ryan AbilityLab (formerly Rehabilitation Institute of Chicago) and Dr. Michelle Gittler and Dr. Ray Lee at Schwab Rehabilitation Hospital for their support in our recruitment efforts. We would also like to thank Matthew Giffhorn, Dr. Elaine Gregory, Kendra Harmon, Amy Lange, Julia Marks, Dr. Amanpreet Saini, Bernard Stephens, and Renita Yeasted for their help with recruitment and data collection.

Funding

This research was supported by Department of Defense U.S. Army Medical Research and Materiel Command (Grant Numbers SC090010 and SC130125). REDCap is supported at FSM by the Northwestern University Clinical and Translational Science (NUCATS) Institute. Research reported in this publication was also supported, in part, by the National Institutes of Health’s National Center for Advancing Translational Sciences (Grant Numbers UL1TR001422 and UL1TR000150). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

Authors and Affiliations

  1. Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, Calgary, AB, T2N 1N4, USA

    I.T. Haider, S.M. Lobos & W.B. Edwards

  2. McCaig Institute for Bone and Joint Health, Cumming School of Medicine, University of Calgary, Calgary, AB, T2N 1N4, USA

    I.T. Haider, S.M. Lobos & W.B. Edwards

  3. Department of Physical Medicine and Rehabilitation, Northwestern University Feinberg School of Medicine, Chicago, IL, 60611, USA

    N. Simonian & T.J. Schnitzer

  4. Northwestern University Clinical and Translational Sciences Institute, Northwestern University Feinberg School of Medicine, Chicago, IL, 60611, USA

    N. Simonian

  5. Department of Physical Medicine and Rehabilitation, Rehabilitation Institute of Chicago (d.b.a. Shirley Ryan AbilityLab), Chicago, IL, 60611, USA

    T.J. Schnitzer

Authors
  1. I.T. Haider
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S.M. Lobos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. Simonian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T.J. Schnitzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. W.B. Edwards
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I.T. Haider.

Ethics declarations

Conflicts of interest

None.

Electronic supplementary material

Figure A1

Segmentation of representative slices from a distal femur. Simple thresholding (GREEN) was used to identify the periosteal boundary. Some manual clean-up (PURPLE) was required to fill any gaps. Image slices at the epiphysis (TOP) required more manual effort compared to slices at the diaphysis (BOTTOM). (JPG 71 kb)

Figure A2

Representative FE model of the distal femur (TOP) and proximal tibia (BOTTOM) generated from one participant. Each bone was separated into three models, representing the epiphysis, metaphysis and diaphysis. The undeformed shape, and boundary conditions are shown on the LEFT. One end was full fixed (RED) while loads were applied to a reference point (WHITE CIRCLE). The model was then patient to torsion (MIDDLE) and axial compression (RIGHT). For clarity, the torsional and axial deformations shown are exaggerated by a factor of 15 and 10, respectively. (JPG 389 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Haider, I., Lobos, S., Simonian, N. et al. Bone fragility after spinal cord injury: reductions in stiffness and bone mineral at the distal femur and proximal tibia as a function of time. Osteoporos Int 29, 2703–2715 (2018). https://doi.org/10.1007/s00198-018-4733-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-018-4733-0

Keywords

Search

Navigation