Skip to main content
Log in

Changes in Bone Mass, Bone Structure, Bone Biomechanical Properties, and Bone Metabolism after Spinal Cord Injury: A 6-Month Longitudinal Study in Growing Rats

  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

Spinal cord injury (SCI) results in a great decline in bone mineral density (BMD) and deterioration of bone microarchitecture. The objective of this study was to investigate the time course of the changes in BMD, microarchitecture, biomechanical properties, and bone turnover in male growing rats following SCI. Sixty male growing Sprague-Dawley rats, 6 weeks of age, were randomly divided into SCI (lower thoracic cord transection) and sham-operated groups, and bone tissues and blood samples were examined at 3 weeks, 6 weeks, and 6 months after surgery. SCI rats had low bone weight (wet, dry, and ash weight) and BMD of the femora, tibiae, and third lumbar vertebrae at all time points compared to sham rats, while in forelimbs, there was a decrease of dry and ash weight compared to sham rats only at 3 weeks but not BMD. Bone microarchitecture and trabecular connectivity were deteriorated in SCI rats and remained so after. Bone formation rate and serum osteocalcin level in SCI rats were significantly increased 3 weeks after SCI surgery. However, eroded surface/bone surface and serum N-terminal telopeptide of type I collagen level remained elevated from 3 weeks to 6 months. In addition, SCI rats showed poor biomechanical properties in the proximal tibiae and femora but not in the humeri. In conclusion, SCI causes profound BMD loss, disturbances in bone microarchitecture, decreased mechanical strength in the lower extremity and lumbar spine, and high bone turnover. These findings will allow better understanding of osteoporosis following SCI.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.

Similar content being viewed by others

References

  1. Frey-Rindova P, de Bruin ED, Stussi E, Dambacher MA, Dietz V (2000) Bone mineral density in upper and lower extremities during 12 months after spinal cord injury measured by peripheral quantitative computed tomography. Spinal Cord 38:26–32

    Article  PubMed  CAS  Google Scholar 

  2. Hill EL, Martin RB, Gunther E, Morey-Holton E, Holets VR (1993) Changes in bone in a model of spinal cord injury. J Orthop Res 11:537–547

    Article  PubMed  CAS  Google Scholar 

  3. Warden SJ, Bennell KL, Matthews B, Brown DJ, McMeeken JM, Wark JD (2002) Quantitative ultrasound assessment of acute bone loss following spinal cord injury: a longitudinal pilot study. Osteoporos Int 13:586–592

    Article  PubMed  CAS  Google Scholar 

  4. Modlesky CM, Majumdar S, Narasimhan A, Dudley GA (2004) Trabecular bone microarchitecture is deteriorated in men with spinal cord injury. J Bone Miner Res 19:48–55

    Article  PubMed  Google Scholar 

  5. Ragnarsson KT, Sell GH (1981) Lower extremity fractures after spinal cord injury: a retrospective study. Arch Phys Med Rehabil 62:418–423

    PubMed  CAS  Google Scholar 

  6. Ingram RR, Suman RK, Freeman PA (1989) Lower limb fractures in the chronic spinal cord injured patient. Paraplegia 27:133–139

    PubMed  CAS  Google Scholar 

  7. Comarr AE, Hutchinson RH, Bors E (1962) Extremity fractures of patients with spinal cord injuries. Am J Surg 103:732–739

    Article  PubMed  CAS  Google Scholar 

  8. Leblanc AD, Schneider VS, Evans HJ, Engelbretson DA, Krebs JM (1990) Bone mineral loss and recovery after 17 weeks of bed rest. J Bone Miner Res 5:843–850

    PubMed  CAS  Google Scholar 

  9. Kiratli BJ, Smith AE, Nauenberg T, Kallfelz CF, Perkash I (2000) Bone mineral and geometric changes through the femur with immobilization due to spinal cord injury. J Rehabil Res Dev 37:225–233

    PubMed  CAS  Google Scholar 

  10. Takata S, Yasui N (2001) Disuse osteoporosis. J Med Invest 48:147–156

    PubMed  CAS  Google Scholar 

  11. Uebelhart D, Demiaux-Domenech B, Roth M, Chantraine A (1995) Bone metabolism in spinal cord injured individuals and in others who have prolonged immobilisation. A review. Paraplegia 33:669–673

    PubMed  CAS  Google Scholar 

  12. Garland DE, Adkins RH, Kushwaha V, Stewart C (2004) Risk factors for osteoporosis at the knee in the spinal cord injury population. J Spinal Cord Med 27:202–206

    PubMed  Google Scholar 

  13. Jiang SD, Jiang LS, Dai LY (2006) Spinal cord injury causes more damage to bone mass, bone structure, biomechanical properties and bone metabolism than sciatic neurectomy in young rats. Osteoporos Int 17:1552–1561

    Article  PubMed  Google Scholar 

  14. Huang TH, Lin SC, Chang FL, Hsieh SS, Liu SH, Yang RS (2003) Effects of different exercise modes on mineralization, structure, and biomechanical properties of growing bone. J Appl Physiol 95:300–307

    PubMed  CAS  Google Scholar 

  15. Alcock N, Macintyre I, Radde I (1960) The determination of magnesium in biological fluids and tissues by flame spectrophotometry. J Clin Pathol 13:506–510

    PubMed  CAS  Google Scholar 

  16. Huang TH, Yang RS, Hsieh SS, Liu SH (2002) Effects of caffeine and exercise on the development of bone: a densitometric and histomorphometric study in young Wistar rats. Bone 30:293–299

    Article  PubMed  Google Scholar 

  17. Bourrin S, Genty C, Palle S, Gharib C, Alexandre C (1994) Adverse effects of strenuous exercise: a densitometric and histomorphometric study in the rat. J Appl Physiol 76:1999–2005

    PubMed  CAS  Google Scholar 

  18. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595–610

    Article  PubMed  CAS  Google Scholar 

  19. Hogan HA, Ruhmann SP, Sampson HW (2000) The mechanical properties of cancellous bone in the proximal tibia of ovariectomized rats. J Bone Miner Res 15:284–292

    Article  PubMed  CAS  Google Scholar 

  20. Lochmuller EM, Miller P, Burklein D, Wehr U, Rambeck W, Eckstein F (2000) In situ femoral dual-energy X-ray absorptiometry related to ash weight, bone size and density, and its relationship with mechanical failure loads of the proximal femur. Osteoporos Int 11:361–367

    Article  PubMed  CAS  Google Scholar 

  21. Garland DE, Stewart CA, Adkins RH, Hu SS, Rosen C, Liotta FJ, Weinstein DA (1992) Osteoporosis after spinal cord injury. J Orthop Res 10:371–378

    Article  PubMed  CAS  Google Scholar 

  22. Zehnder Y, Luthi M, Michel D, Knecht H, Perrelet R, Neto I, Kraenzlin M, Zach G, Lippuner K (2004) Long-term changes in bone metabolism, bone mineral density, quantitative ultrasound parameters, and fracture incidence after spinal cord injury: a cross-sectional observational study in 100 paraplegic men. Osteoporos Int 15:180–189

    Article  PubMed  Google Scholar 

  23. Carter DR, Hayes WC (1977) The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg Am 59:954–962

    PubMed  CAS  Google Scholar 

  24. Majumdar S, Kothari M, Augat P, Newitt DC, Link TM, Lin JC, Lang T, Lu Y, Genant HK (1998) High-resolution magnetic resonance imaging: three-dimensional trabecular bone architecture and biomechanical properties. Bone 22:445–454

    Article  PubMed  CAS  Google Scholar 

  25. Link TM, Majumdar S, Augat P, Lin JC, Newitt D, Lu Y, Lane NE, Genant HK (1998) In vivo high resolution MRI of the calcaneus: differences in trabecular structure in osteoporosis patients. J Bone Miner Res 13:1175–1182

    Article  PubMed  CAS  Google Scholar 

  26. Ciarelli TE, Fyhrie DP, Schaffler MB, Goldstein SA (2000) Variations in three-dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res 15:32–40

    Article  PubMed  CAS  Google Scholar 

  27. Dempster DW (2000) The contribution of trabecular architecture to cancellous bone quality. J Bone Miner Res 15:20–23

    Article  PubMed  CAS  Google Scholar 

  28. Bedbrook GM, Sedgley GI (1980) The management of spinal injuries–past and present. Int Rehabil Med 2:45–61

    PubMed  CAS  Google Scholar 

  29. Kleerekoper M, Villanueva AR, Stanciu J, Rao DS, Parfitt AM (1985) The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif Tissue Int 37:594–597

    Article  PubMed  CAS  Google Scholar 

  30. Majumdar S, Link TM, Augat P, Lin JC, Newitt D, Lane NE, Genant HK (1999) Trabecular bone architecture in the distal radius using magnetic resonance imaging in subjects with fractures of the proximal femur. Magnetic Resonance Science Center and Osteoporosis and Arthritis Research Group. Osteoporos Int 10:231–239

    Article  PubMed  CAS  Google Scholar 

  31. Demulder A, Guns M, Ismail A, Wilmet E, Fondu P, Bergmann P (1998) Increased osteoclast-like cells formation in long-term bone marrow cultures from patients with a spinal cord injury. Calcif Tissue Int 63:396–400

    Article  PubMed  CAS  Google Scholar 

  32. Parfitt AM (1987) Trabecular bone architecture in the pathogenesis and prevention of fracture. Am J Med 82:68–72

    Article  PubMed  CAS  Google Scholar 

  33. Roberts D, Lee W, Cuneo RC, Wittmann J, Ward G, Flatman R, McWhinney B, Hickman PE (1998) Longitudinal study of bone turnover after acute spinal cord injury. J Clin Endocrinol Metab 83:415–422

    Article  PubMed  CAS  Google Scholar 

  34. Maimoun L, Couret I, Micallef JP, Peruchon E, Mariano-Goulart D, Rossi M, Leroux JL, Ohanna F (2002) Use of bone biochemical markers with dual-energy X-ray absorptiometry for early determination of bone loss in persons with spinal cord injury. Metabolism 51:958–963

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This study was supported by the hospital and school of medicine where the authors work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L.-Y. Dai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiang, SD., Jiang, LS. & Dai, LY. Changes in Bone Mass, Bone Structure, Bone Biomechanical Properties, and Bone Metabolism after Spinal Cord Injury: A 6-Month Longitudinal Study in Growing Rats. Calcif Tissue Int 80, 167–175 (2007). https://doi.org/10.1007/s00223-006-0085-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-006-0085-4

Keywords

Navigation